THE JOURNAL OF COMPARATIVE NEUROLOGY 312:353-370 (1991)

Somatotopic Component of the Multisensory Map in the Deep Laminae of the Cat Superior Colliculus M. ALEX MEREDITH, H. RUTH CLEMO, AND BARRY E. STEIN Departments of Anatomy (M.A.M.) and Physiology (H.R.C., B.E.S.), Medical College of Virginia, Virginia Commonwealth University, Richmond, Virginia 23298-0709

ABSTRACT The topographic organization of the somatosensoryrepresentation in the deep layers of the cat superior colliculus was reexamined using methods previously used to examine the visuotopy in these layers. This technique identified the distribution of neurons in the superior colliculus that represent a designated region of the body surface (i.e., a dermal image), as well as assessed the differential distribution of deep layer neurons representing different body regions (e.g., face, forelimb, hindlimb, etc.). When the area of densest representation within a dermal image was considered, a well-ordered somatotopy was evident that was similar to the one previously described (Stein et al., '76: J. Neurophysiol. 39:401419).Each region of the body surface, however, was represented within a surprisingly broad area of the deep layers, which often had considerable overlap with the representations of adjacent body regions. This organization was similar to that of the deep layer visuotopy and emphasizes that the representation of a peripheral stimulus is accomplished by the simultaneous activation of a large population of deep layer neurons. Furthermore, an examination of the convergencepatterns on somatosensoryresponsive neurons demonstrated that the somatotopy was formed primarily by multisensory neurons. These data indicate that the somatosensory representation is best considered as a component of a comprehensive multisensory functional unit that plays a critical role in effecting behavioral responses to a wide variety of stimuli. Key words: somatosensory,visual, auditory, multirnodal, receptive field

Unlike nuclei along the primary sensory pathways, the deep layers of the superior colliculus do not separate representations of different sensory modalities from one another. It does quite the opposite, and it is because of the intermixing of visual, auditory, and somatosensory modalities that the deep layers (below stratum opticum) have been designated "multisensory" (for review, see Stein, '84). Not only do neighboring neurons respond to stimuli from different sensory modalities, but many of the same neurons receive convergent inputs from the different sensory systems (e.g., Stein and Arigbede, '72; Gordon, '73; Drager and Hubel, '75, '76; Stein et al., '76; Chalupa and Rhoades, '78; Finlay et al., '78; Graham et al., '81; King and Palmer, '85; Meredith and Stein, '86a,b). A distinctive feature of many of these multisensory neurons is the general spatial alignment of the receptive fields of each modality (Gordon, '73; Stein et al., '76; Drager and Hubel, '76; Chalupa and Rhoades, '78; Middlebrooks and Knudsen, '84; King and Palmer, '85; Meredith and Stein, '86a). Collectively, these receptive fields constitute the spatiotopic maps found in this structure. Recently, the deep layer map of visual space has been shown to be composed largely of multisensory

o 1991 WILEY-LISS. INC.

neurons (Meredith and Stein, '901, suggesting that the visual map is but one component of an integrated multisensory map. If so, one might expect that the same is true of the somatosensoryrepresentation. The primary objective of the present experiments was to examine this possibility by determining whether the somatotopicmap (Stein et al., '76) is composed of multisensory neurons (i.e., neurons responsive to somatosensory and nonsomatosensory stimuli). A second objective was to reevaluate the somatotopicmap in a manner compatible with that used to demonstrate the deep layer visuotopic map (Meredith and Stein, '90). Like deep layer visual and auditory receptive fields, many somatosensory receptive fields are large (Gordon, '73; Stein et al., '76; Nagata and Kruger, '79; Clemo and Stein, '84, '86, '87; Clemo and Stein [in press]; Meredith and Stein, '86b), suggesting that a punctate cutaneous stimulus can directly activate a widespread area of the structure. The construcAccepted July 9,1991. Address reprint requests to M. Alex Meredith, Dept. of Anatomy, Medical College of Virginia, Virginia Commonwealth University, Box 709 MCV Station, Richmond,VA 23298-0709.

M.A. MEREDITH ET AL.

354 tion of “dermal images” (modified from “point images,” see McIlwain, ’75; Meredith and Stein, ’90) is a method that lends itself to examining this possibility. A brief report describing these experiments has been presented in abstract form (Meredith et al., ’90).

MATERIALS AND METHODS Data were obtained using standard extracellular recording techniques that have been described in detail in a previous report (Meredith and Stein, ’86b). All procedures were performed in compliance with the Guide for the Care and Use of Laboratory Animals (NIH Publication No. 86-23) at Virginia Commonwealth University, which is accredited by the American Association for Accreditation of Laboratory Animal Care (AAALAC).

Surgical preparation Approximately 1week prior to the first recording session, each cat (n = 21) was anesthetized with sodium pentobarbital(40 mglkg, with supplements of 5-10 mglkg, i.v.), and placed in a stereotaxic head-holder. Aseptic conditions were maintained while a 2-cm craniotomy was made to expose the cortex dorsal to the superior colliculus, and a hollow cylinderlhead-holdingdevice was implanted over this opening.

Recording

posterior (AP)and medio-lateral (ML) extent of the superior colliculus (e.g., 35% from caudal end, 72% from midline), and transferred to a representative tracing of a coronal section through the superior colliculus.

Evaluation of sensory convergence and receptive field mapping As the electrode was lowered through the superior colliculus, somatosensory-responsiveneurons were sought using air puffs, stroking and tapping the body surface with a small brush, manipulating subcutaneous tissues, and joint rotation. Once a neuron responsive to somatosensory stimulation was identified, its activation by inputs from other modalities was tested using a variety of auditory (hisses, claps, whistles) and visual (bars or spots of light projected from a hand-held pantoscope were flashed or moved across a translucent plexiglass hemisphere positioned in front of the animal) stimuli. If a neuron was unresponsive to these stimuli presented individually, the possibility that they had subthreshold influences was examined by presenting electronically-generated somatosensory-auditory and somatosensory-visual stimulus combinations (see Meredith and Stein, ’86b). Somatosensory neurons that were either excited or inhibited by stimuli from other modalities were classified as “multisensory,” whereas those neurons unaffected by other stimulus modalities were considered “somatosensory-unimodal.’’ Once a somatosensory-responsiveneuron was identified, its force threshold was determined with a von Frey hair and this minimal stimulus was used to map its receptive field. In the case of hair-activated neurons, the von Frey hair was used to move small numbers of guard hairs. Each receptive field was plotted on a scaled drawing of the body surface. This drawing was obtained by tracing a photograph of an adult male cat (3.2 kg).

Despite the absence of wounds or pressure points, all recording experiments were conducted with animals anesthetized with ketamine hydrochloride (30 mg/kg, i.m.). The animal was intubated through the mouth, paralyzed (pancuronium bromide, 10 mglkg, i.v., subsequent doses 0.6-0.8 mg/kg, i.v.), and ventilated with 25% 0, and 75% N,O. Paralysis was required to stabilize eye position necessary for concurrent experiments regarding the representation of the visual modality in this same structure (see Meredith Data analysis and Stein, ’90). Subsequent doses of anesthetic (10-15 Graphic, scaled representations of somatosensory recepmglkglhr, i.v.), sufficient to maintain anesthesia in nonparalyzed preparations, were delivered routinely. The effective- tive fields were used to examine the deep layer somatotopy ness of this regimen was checked periodically during each and the relationship of receptive field size to neuronal experiment by permitting the animal to recover from location. Receptive field size was measured directly from paralysis. Expiratory CO, was kept between 3.7 and 4.5% the scaled drawing using a Zeiss MOP-3 digital planimeter. and body temperature was maintained at 37-38°C with a No attempt was made to compensate, on the two-dimensional forms, for curvatures of the body surface or at skin heating pad. The recording well was fitted with a calibrated X-Y slide folds such as those in the pinnae or on the footpads. for the positioning of each electrode penetration and the Therefore, these receptive field measures represent only an activity of single neurons was recorded with glass-insulated approximation of the actual area occupied by a given tungsten electrodes (impedance 2 1 MOhm at 1 kHz, receptive field and are used to make relative comparisons. 12-20 pm tip exposure). Electrodes were advanced with a Values for receptive field area as well as neuronal position hydraulic microdrive and the depth of neurons along a (depth, AP-,ML-location) and pattern of modality converpenetration was noted. Successful recording penetrations gence (unimodal, somatosensory-visual, somatosensory15 sec) and auditory, trimodal) were entered into a VAX computer and were marked with electrolytic lesions (12 d, the positions of recorded neurons were later located histo- correlations among these different variables were obtained using statistical correlation procedures. logically. The deep layer somatotopy was examined by identifying At the end of an experiment, paralytics, and then anesthetics, were discontinued. The animal was then weaned from the distribution of recording sites whose receptive fields the ventilator and was returned to its home cage after occupied a specified subdivision, or region, of the body regaining respiratory and locomotive functions. At the surface. These dermal regions were the cranium, face, conclusion of a series of recording sessions (usually no vibrissa pad, chin, forepaw, forelimb (including shoulder), greater than four), the animal was euthanized with an back, trunk, ventrum (including belly, chest, and ventral overdose of barbiturate and perfused with physiological surface of forelimb and hindlimb), hindlimb, and tail. For saline and 10% formalin. The midbrain was blocked and example, to establish where the representation of forepaw was processed using routine histologicalprocedures (50 pm was located in the tissue, the location of each neuron whose frozen sections, cresyl violet staining). Neuronal locations receptive field included or encroached on the forepaw was were determined to the nearest percentage of the anterior- plotted at the appropriate anterior-posterior (AP)and

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SOMATOTOPY IN DEEP SUPERIOR COLLICULUS medial-lateral (ML) position on a standardized horizontal section through the stratum griseum intermediale (as determined by acetylcholinesterase staining [Dunning et al., ,871). The distribution of all the neurons plotted in this manner was then defined as the representation, or the dermal image, of the forepaw in the superior colliculus. This process was repeated for each of the other regions of the body. Two other similar measures also were used to examine the organization of the somatosensory representation in the superior colliculus. Because the representation of a given body region is not homogeneous within its dermal image, we devised one method by which the density of the representation was measured (Meredith and Stein, ’90). By using the criterion of the inclusion of a specifiedbody region in 2 75%of the receptive fields per penetration, a representational focus for that body region could be identified. Thus by plotting the AP-ML location of only those penetrations that met the 2 75% criteria, a “best dermal image” was constructed for each body region. In addition, because some receptive fields fell exclusively within a given body region, “exclusive dermal images” were made in a similar fashion by plotting the AP-ML location of neurons whose receptive fields were entirely contained within a specified body region. Finally, by applying these same dermal imaging techniques to plots made on serially arranged coronal sections, the vertical extent of the somatosensory representation across laminae also was examined. The relative proportion of the superior colliculus occupied by each best dermal image was measured using the Zeiss Digital MOP-3 Planimeter and then divided by the area of the superior colliculus (measured in the same fashion from a horizontal section through the stratum griseum intermediale). The same instrument was also used to determine the area of the different body regions (defined above) from the graphic representation of the cat (see above). Finally, the relative magnification of the representations of the different body regions within cat primary somatosensory cortex was determined with the same device from the published figures of Felleman et al. (’83).

’84, ’86, ’87; Meredith and Stein, ’86b). Furthermore, the overwhelming majority (96%)of them had receptive fields confined to the contralateral body, and it was only the rare receptive field (101230) that crossed the midline. Of these bilateral receptive fields, the ipsilateral portions always included the face and most often (6/10) included some part of the perioral zone. Eight receptive fields were encountered that differed markedly from the rest: two encompassed the entire body surface and six had discontinuous receptive fields with clearly delimited, unexcitable intervening areas.

Receptive field size: Influence of neuronal location Somatosensory-responsiveneurons were encountered as soon as the electrode reached the intermediate gray layer and were found throughout all deep laminae. Within a given electrode penetration, the receptive fields of somatosensory-responsive neurons tended to cluster about a single region of the body (e.g., forelimb, head, etc.) but exhibited considerable variability in size. The example presented in Figure 1was typical. All receptive fields in this electrode penetration encroached on some portion of the forelimb, but some were restricted to the forepaw and others included the trunk and/or hindlimb. The variability in receptive field size and their spread across different body regions was not predictable on the basis of the depth at which a neuron was found, or the lamina in which it was located (Fig. 2). Although most (52%)of the receptive fields were 5 100 cm’, at any given depth within the superior colliculus receptive fields could be small (coveringa portion of a given body region) or large (covering more than one body region). Thus there was no correlation (r = 0.025, linear regression) between receptive field size and the location of a neuron along an electrode track.

Receptive field size: Variation with rostrocaudal location

The somatotopic map in the deep superior colliculus has been described earlier in terms of the representation of body sectors (Stein et al., ’76). This study reported that the Response quantification and head was represented rostral and the hindlimb was caudal multisensory tests in the tissue and that changes in receptive field sizes were These procedures have been described in detail in a “related to innervation density” of the cutaneous surface. previous report (Meredith and Stein, ’86b) and are only In the present study, these same trends were noted within summarized here. Electronically-controlled somatosen- the overall sample as well as within individual animals, as sory, visual, and auditory stimuli were repeatedly presented shown in Figure 3. Furthermore, there was a general alone, and in combination, in an interleaved fashion. Stimu- tendency for receptive fields of neurons located in the lus combinations were configured to be spatially coincident, rostral sectors of the superior colliculus to be smaller than or within the excitatory receptive fields of the neuron, and those found caudal. This gradient (r = 0.48, linear regreswere programmed to occur within 50 ms of one another. sion) may be due to the segregation of the smaller receptive Neuronal responses to these tests were stored on a PDP fields within the rostral two-thirds of the structure, where 11/23 computer, which generated rasters and peristimulus- the face and forepaw are represented (see below). However, time histograms as well as executed statistical analyses large receptive fields that encompassed most, if not all, of (mean, standard deviation, standard error). the contralateral body surface were observed in neurons found throughout the rostral-caudal extent of the superior colliculus. In addition, the likelihood of a receptive field RESULTS being restricted to a single body region depended on its A total of 230 neurons responsive to somatosensory rostrocaudal location on the body. Receptive fields on the stimuli were studied in the deep layers of the cat superior head had the highest probability of being restricted to that colliculus. In agreement with previous observations, all of portion of the body (42%)and had a lower probability (27%) these neurons were readily activated by low-threshold of expanding to include the hindlimb. In contrast, only 4% cutaneous stimulation, responded best to intermediate- of hindlimb receptive fields were contained within that body high velocity stimuli, and were rapidly adapting (e.g., see region and more than ten times as many (43%)expanded to Stein et al., ’76; Nagata and Kruger, ’79; Clemo and Stein, include portions of the head (see Table 1).

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I

Fig. 1. Somatosensory receptive fields (right) mapped at specific locations (hashmarks) within a single electrode penetration through the superior colliculus (left). Midline is to the left of this cresyl violet-stained section. The pattern of modality convergence is denoted by the letters to the right of each receptive field (S = somatosensory

only; SV = somatosensory-visual), but only somatosensory receptive fields are depicted. SGS = Stratum Griseum Superficiale; SO = Stratum Opticum; SGI = Stratum Griseum Intermediale; SAI = Stratum Album Intermediale; SGP = Stratum Griseum Profundum; S A P = Stratum Album Profundum.

0--- Unimodal

U----Unimodal M --Multisensory

Multisensory

0 C

E 4 5 \ u)

c

2

n

z

SAP 1

0

500

1000

I500

0

500

-

1

I

1000

Receptive Field Area (cm2) Fig. 2. The relationship of receptive field area and neuronal depth within the superior colliculus. There was little correlation among receptive field area and depth below the surface (A) or lamina (B). Also, unimodal somatosensory neurons (U) were intermingled with multisensory neurons (M) at all depths. Laminar abbreviations are the same as Figure 1.

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SOMATOTOPY IN DEEP SUPERIOR COLLICULUS

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Fig. 3. Receptive fields mapped alongfive different electrode penetrations within the same superior colliculus showed a general yet consistent shift in relation to recording site. The position of each recording site (filled circles) is indicated on the dorsal view of the superior colliculus (left), and the corresponding receptive fields are shown in the order in which they were encountered.Rostral recording sites tended to

yield receptive fields on the face; more caudal locations had receptive fields on the body, and those located laterally had receptive fields on the forelimb or paw. The pattern of modality convergence is shown below each receptive field, where S = somatosensory only, SV = somatosensory-visual,and SAV = somatosensory-auditory-visual.

TABLE 1. Receptive Field ExpansioniRestrictionVersus Location

’901, was used to map the somatosensory representation. “Dermal images” were constructed by delimiting the distribution of all neurons whose receptive fields included any portion of the same body region. As might be expected, and as can be seen from Figure 4,these dermal images were quite large. For example, neurons whose receptive fields included the head (i.e., those with receptive fields only on the head as well as those in which the head was included in a larger receptive field) could be found in all but the most caudal aspects of the superior colliculus, whereas those with receptive fields on the body also showed a widespread distribution except that they were excluded from the rostral pole. These observations indicate that the general representation of any body region occupies an extremely broad area of tissue. To examine the resolution of the somatosensory representation, two additional forms of dermal images were mapped: the “best dermal image” (defined as the area in which 2 75% of the receptive fields per penetration shared a given body region), and the “exclusive dermal image” (defined as the area of tissue containing receptive fields devoted exclusively to a given body region). All three of these dermal images are presented in a comparison of the representations of head versus body in Figure 4. As might be expected, the more restrictive criteria used in the analysis of best and exclusive dermal images yielded more restricted blocks of

Head Forelimb Trunk Hindlimb

Head

Forelimb

Trunk

42%’ 39% 47% 43%

55% 52%’ 94% 90%

Hindlimb

Total Number

38%

27%

54%

40% 69% 4%’

n = 107 (46.5%) n = 149 (64.8%) n = 87 (37.8%) n = 67 (29.1%)

0%2

90%

The proportion of receptive fields found in the body regions listed in the column (left) that were restricted to or expanded to include the body regions designated at the top. Progressively more caudal receptive fields include more body regions, whereas the more rostral the receptive field, the more likely it was to be restrictedto a single body region. Since many receptive fields encompassed more than one body region, total percentages are greater than 100%. Due to the manner in which the data wa8 computed,values should be read along rows, not down columns. ‘Denotesthat receptive fields are restricted to that body region and is not a measure of all receptive fields that include the stipulated body part.

Dermal images and the deep layer somatotopy Just as the largeness of the visual receptive fields in deep superior colliculus precludes a point-to-point visuotopy (Meredith and Stein, ,901, the large size of somatosensory receptive fields seems to preclude a point-to-point somatotopy. Furthermore, the large somatosensory receptive fields make it likely that points on the body surface have access to a wide expanse of the superior colliculus. In order to determine the area of tissue representing a given region of the body, a procedure analogous to the visual “pointimage” technique (McIlwain, ’75), used previously to detail the deep layer visual representation (Meredith and Stein,

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358

Al I

Exclusive

k 75%/Penetration

Head

Body

,s9 %

Caudal

I mm

Fig. 4. A somatotopy is especially apparent when the density, or exclusivity, of representation of a given body region is considered. Neurons with receptive fields that encompass the head (top) or body (bottom) can be found throughout the entire extent of the superior colliculus (All-left).However, when these same data are examined with respect to the proportion of receptive fields that include a specified body

region per penetration ( t 75%/penetration-center) or are restricted to a body region (exclusive-right),a somatotopy becomes apparent. These three categories are referred to as a “dermal image” (left), “best dermal image” (center), and “exclusive dermal image” (right). Filled circles represent penetrations that met the criteria stipulated at the top of the column; dashes indicate penetrations that did not.

tissue and a more highly resolved and detailed somatotopy. This held for each of the body regions examined (Fig. 5A,B,C). By using measures of either best or exclusive dermal images, it was apparent that tissue devoted primarily to the cranium, face, vibrissa pad, and chin were reasonably well defined within the rostral half of the superior colliculus and progressed from medial to lateral, respectively, across the structure (see Fig. 5A). Similarly, the dorsal-to-ventral axis along the trunk was represented in a medial-to-lateral progression in the caudal half of the structure as shown in Figure 5B (although no exclusive dermal image for the trunk was found). The representation of the limbs (forelimb extending more rostral than hindlimb) and tail (most caudal) are shown in Figure 5C, and a comparison of the different territories devoted to the various body regions and the overlap among them is illustrated in Figure 6. This summary figure illustrates the general somatotopic plan, and its axes, found in the superior colliculus: the head is represented rostral; the body and tail caudal; upper body parts are medial; lower/ventral body parts are lateral. To determine if the different dermal images might occupy distinct laminar territories within the deep layers, the data for each region of the body were replotted on a sequence (spaced 450 p,m apart) of coronal sections. Figure 7 shows a representative sample of these analyses, which revealed that the dermal images were never restricted to a specific lamina but spanned the full thickness of the deep layers. The representation of the face and forelimb appear to occupy far more tissue than would be expected on the basis of the size of their cutaneous distribution. Thus whereas

the head accounts for approximately 8% of the body surface, its best dermal image occupies half (50.6%) the area of the superior colliculus. Similarly, whereas the forepaw includes only 1.5% of the body surface, its best dermal image occupies a much greater proportion (27%)of the deep layers. In contrast, relatively large body parts such as the trunk and hindlimb (which occupy 26%and 22% of the body surface, respectively) have considerably smaller areas of representation (19% and 9%, respectively) in the superior colliculus. The striking nature of the magnification of some body regions and the constriction of others in this somatotopy is graphed in Figure 8A,B. Despite the fact that even a single point within any one of these body regions is represented by at least some neurons that are distributed across a major portion of the superior colliculus (e.g., see Fig. 4),the density of involved neurons falls off sharply as one moves away from the area of the best dermal image. As shown in Figure 9, this produces a focus of representation for each region of the body that most often is distinct from the others. Thus whereas the dermal image of the face covers nearly the entire structure, its focus is in the rostral half of the superior colliculus, which is discernable from the focus of representation from the forepaw and the hindlimb (see Fig. 9).

Somatotopy: One component of a multisensory map After mapping the receptive field of a somatosensoryresponsive neuron, nonsomatosensory (i.e., visual and auditory) stimuli were presented to determine whether it was

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SOMATOTOPY IN DEEP SUPERIOR COLLICULUS

A

Al I

575% /Penetration

Exclusive

\

Chin

Caudal

I mm

Fig. 5. Dermal- (All), best dermal- ( 2 75%/penetration) and exclusive dermal images of the different body regions. A (above).Whereas the dermal images of the cranium (top) to the chin (bottom) cover nearly the entire superior collieulus, best- and exclusive dermal images are

much more restricted and parallel one another: they progress from medial to lateral in the structure as the body region shifts dorsal (cranium) to ventral (chin). Symbols as in Figure 4.

multisensory. Although exhaustive tests with each possible visual and auditory stimulus could not be done and the present sample may represent an underestimation, the majority (145/230, 63%) of the somatosensory-responsive neurons were found to be multisensory since they also received visual andlor auditory inputs. The proportion of neurons falling within each of the various sensory convergence patterns is presented in Table 2.

The somatosensoryproperties of multisensory somatosensory-responsiveand unimodal somatosensory neurons were essentially the same, and each group was dominated by inputs with intermediate to high velocity thresholds from hair receptors. The only apparent difference was that multisensory neurons had significantly (t = 2.5, df = 228, p < 0.001, t-test) larger somatosensory receptive fields than did unimodal neurons (see Table 2). Furthermore,

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Exclusive

Vent r um -

--

\

Fig. 5. B. Similarly, images of the body regions from the back (top) to the ventrum (bottom) change progressively from medial to lateral as receptive fields shift from dorsal to ventral.

there was a significant (t = 4.35, df = 143, p < 0.001, t-test) difference in the size of somatosensory receptive fields between bimodal and trimodal neurons. Even though numerous unimodal somatosensory neurons were encountered, the majority of neurons found in each dermal image were multisensory (Fig. 10). Since unimodal and multisensory somatosensory-responsiveneurons contribute differently to the formation of dermal images, each dermal and best dermal image was reconstructed according to locations of its unimodal or multisensory neurons. As can be seen from Figure 11, no dermal image, or best dermal image, was composed completely of either type of neuron, and the distribution of multisensory and unimodal neurons within these images is strikingly similar and often coextensive. However, it is clear that multisensory neurons form the major population within each dermal image and best dermal image. Because the neurons that constitute the map of the body in the superior colliculus are largely multisensory, the somatotopy reflects only one dimension of these multisensory neurons. Whenever possible, the visual and/or auditory receptive fields of these multisensory somatosensory-respon-

sive neurons were also mapped, and, as has been documented earlier (Gordon, '73; Middlebrooks and Knudsen, '84; King and Palmer, '85; Meredith and Stein, '86a),the different sensory receptive fields for a given neuron showed a general spatial register. An example of the registry of different receptive fields in three multisensory neurons from a single animal is presented in Figure 12. In these and other cases, the locationsof the somatosensoryand nonsomatosensory receptive fields are dependent on the neuronal position within the superior colliculus and vary according to the organization of their related sensory map. Thus the somatosensory receptive fields of multisensory neurons found rostral in the superior colliculus were most often found on the face, whereas their visual receptive fields included the projection of the area centralis. Similarly, multisensory neurons found in the most caudal aspects of the structure had somatosensory receptive fields on the trunk and hindlimb and visual receptive fields in far temporal visual space. Thus because multisensory neurons (whosedifferent receptive fields are in register) make up the different deep layer maps, the somatosensory and nonsomatosensory representations should, and do, exhibit spatial covariance.

SOMATOTOPY IN DEEP SUPERIOR COLLICULUS

C

All

361

.-Xi%/Penetration

Exclusive

Forepaw

Fore1imb

HindI imb

Tai I

rn Fig. 5 C. Images of the body regions from forepaw (top) to tail (bottom) shift systematically from rostro-lateral to caudal as receptive fields become progressively more caudal.

A likely consequence of the alignment of somatosensory and visual receptive fields would be to permit responses from causally related stimuli (i.e., the tactile pressure and the sight of an insect on the body) access to the same neuron whereupon the responses to the different stimuli are integrated (Meredith and Stein, '86a). This possibility was tested in multisensory somatosensory neurons by presenting electronically controlled stimuli from each modality within their excitatory receptive field. These stimuli were either presented alone, or in combination with each

other, and the different conditions were interleaved. Whereas the somatosensory and the nonsomatosensory stimuli alone were effective in driving the neurons, combining the different stimuli yielded responses that were significantly greater than those evoked by either stimulus alone, as shown for other multisensory superior colliculus neurons (Meredith and Stein, '83,'85, '86a,b). A representative example of how the responses of a neuron to a somatosensory stimulus is dramatically enhanced by the concurrent presence of a visual stimulus is shown in Figure 13.

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Face

Cranium

Vibrissa Pad

Chin

I mm

Axes

Head

I

Body

I mm

Forelimb

Fig. 6. A summary of the best dermal images for regions on the head (top) and body (bottom) includes the body axes in relation to the somatotopy within the superior colliculus (axes-center). The head is represented primarily in the rostra1 half of the structure and the body

in the caudal half, but both are arranged so that their more superior aspects are represented medial in the superior colliculus; more inferior regions are represented lateral. Note the lateral and caudal locations of the representation of the ventral surfaces of the forelimb and hindlimb.

DISCUSSION

organization of the superior colliculus. Here there are large receptive fields and extensive areas of overlap in the representations of the different body regions. These characteristics were factored into the present study by examining the somatotopy through the use of dermal images. A "dermal image" defines the area within a neural structure to which a region of the body surface has access. This methodology is essentially the same as that used to examine the visuotopy in the superficial (McIlwain, '75) and deep layers (Meredith and Stein, '90) of the superior colliculus. In each case the technique reveals that a broad swath of tissue represents a portion of the peripheral receptor sheet. Because the dermal images include all neurons whose receptive fields encroach on the same portion of the skin and many of the receptive fields are large, it gives only a weak indication of a somatotopy. When,

Deep layer somatotopy A somatotopic organization in the deep layers of the superior colliculus of the cat (Stein et al., '76) and other species (Drager and Hubel, '75; Finlay et al., '78; Stein and Gaither, '81; McHaffie et al., '89) has been demonstrated previously. However, one consequence of descriptions of somatotopic representations anywhere in the brain is to give the impression that there are exclusive domains for different body regions within the representation. Thus the neurons representing the nose are segregated from those representing the tail, and a stimulus within either body region thereby produces a well-defined, spatially limited focus of activity. Although this may be a reasonable approximation of what occurs in primary somatosensory cortex (i.e., Felleman et al., '831, it is an inaccurate depiction of the

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SOMATOTOPY IN DEEP SUPERIOR COLLICULUS

Cranium

ForeI i mb

Vibrissa Pad

\

rJ

Hindlimb

I

Fig. 7. The somatotopy extends through the depth of the deeper laminae of the superior colliculus. Coronal sections taken at regular intervals (450 pm) through the superior colliculus are arranged from rostra1 (top) to caudal (bottom). Dots indicate neurons whose receptive fields include the body region specified at the top of each column,

whereas dashes denote that the designated body region was not contained within the neuron’s receptive field. Each column of tissue sections is identical except that the differential distribution of dots reveals the systematic shift in dermal image location with regard to the representation of the different body regions.

however, only small receptive fields (where the receptive fields are restricted to the same body region) are plotted 6e., “exclusive dermal images”), or representation-density is taken into account by mapping “best dermal images”

(where at least 75% of the neurons in a given electrode penetration must be activated from the same body region), the resolution of the somatotopy is enhanced and its features emerge. The best dermal image of the head

364

M.A. MEREDITH ET AL.

A.

60-

H e a d : Body I

50

-

0 40-

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30-

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> Fig. 8. The magnification of the representation of the different body regions. Despite the differences in the size of the head and the body, their representations occupy nearly equal areas of the superior colliculus. This magnification of the representation of the head and its subdivisions(i.e., cranium, chin, etc.) is presented as a proportion of the

area of the superior colliculus (A) and as a factor of the area of the superior colliculus occupied as a proportion of their surface area (B). Note that the most magnified representations are the vibrissal pad and forepaw.

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SOMATOTOPY IN DEEP SUPERIOR COLLICULUS

Forepaw

Face

Hind1im b

Fig. 9. The focus and distribution of a dermal image are different for each body region. Here, the superior colliculus is divided into 25 sectors and shown in perspective to admit a third axis: the percent of neuronsisector representing a specified body region. On the left, most

sectors contain neurons that have receptive fields on the face, hut only rostral sectors have a high concentration of them. In contrast, neurons with receptive fields on the forepaw or hindlimb are concentrated lateral (center) and caudal (right),respectively, in the structure.

TABLE 2. ConvergencePattern, Incidence,and Receptive Field Area of Somatosensory-responsive Neurons

resembles more closely the organization of the principal somatosensory corticotectal source, S N (Stein et al., '83; Clem0 and Stein, '84, '86) and its deep layer visual and auditory counterparts (Middlebrooks and Knudsen, '84; Meredith and Stein, 'go), than the somatotopy in SI (e.g., see Felleman et al., '83) or the overlying visuotopy in superficial layers (e.g., see Feldon et al., '70; Meredith and Stein. '90).

Convergence pattern Unim odal Multisensory Visual-somatosensory Auditory-somatosensory Visual-auditorv-somatosensorv

Number

MeanAj-ea (range) (cmz)

85

239 (1-938)

87 18 40

357 (3-992) 602 (7-2.287)

G'J'~)

Somatosensory receptive field size occupies the rostral half of the superior colliculus,with the representations of the cranium, face, vibrissa pad, and chin arranged medial-to-lateral within this area. The best dermal image of the body is in the caudal half of the structure, with the forelimb, trunk, hindlimb, and tail represented in a progressively rostral-to-caudal manner. Upper body regions are medial and lower ones are lateral, with the ventrum represented in the most lateral aspect of the structure. Although these general organizational features are fundamentally the same as those described by Stein et al. ('76), additional components of the map have now been revealed, including the representation of the chin, ventral surface of the body and limbs, and the tail. In addition, the distribution of neurons in the superior colliculus representing restricted portions of the cutaneous surface have now been evaluated. These data demonstrate that the best dermal image constitutes a dense representational focus, which falls off as one moves away from this point. These focal areas of representation can be quite large, sometimes occupying as much as 38% of the superior colliculus. Furthermore, each exhibits a considerable degree of overlap with neighboring representations of adjacent body regions. In fact, since no hindlimb receptive fields were found that did not also include trunk, the best dermal images of these two areas were nearly coextensive. Altogether, these observations indicate that the somatotopy in the superior colliculus conforms more closely to a "blocklike" organization than a "point-to-point'' organization. In this sense, it

It is likely that the large size of most superior colliculus somatosensory receptive fields reflects the combined influence of the convergence of afferent fibers and the dendritic extent of superior colliculus neurons. Ascendingsomatosensory afferents arise from the trigeminal and dorsal column nuclei, lateral cervical nucleus, and the spinal cord, where receptive fields rarely occupy more than a portion of a single body region (Baleydierand Mauguiere, '78; Blomqvist et al., '78; Edwards et al., '79; Berkley et al., '80; Huerta et al., '81; Ogasawara, '81; Ogasawara and Kawamura, '82; Rhoades, '81; Cooper and Dostrovsky, '85). Similarly, descending cortical inputs from SIV and para-SIV infrequently demonstrate receptive field sizes on the order of those found in the superior colliculus and descending cortical neurons always had receptive fields that were included within those of their superior colliculus targets (Clemo and Stein, '86). This high degree of convergence no doubt is facilitated by the extensive dendritic arborizations exhibited by many deep layer neurons (Moschovakis and Karabelas, '85). However, even the largest of these (up to 1,400 pm) span only a portion of the entire map and cannot solely account for some of the hemibody receptive fields found here. Therefore, the factors of extensive afferent convergence and expansive dendritic arborizations must interact to account for the size of deep layer somatosensory receptive fields. The functional significance of these large receptive fields may reside in their ability to provide more input from the body surface per unit area of neural tissue. Thus while

M.A. MEREDITH ET AL.

366

0

Fig. 10. Each dermal image is primarily composed of multisensory neurons. These percentages range from > 80% (back, cranium, tail) to 55% (ventrum).

sacrificing spatial resolution within individual receptive fields (but also see below), the general effect of large receptive fields is to enhance the detecting ability of the overall structure. Large receptive fields may perform an additional function in multisensory neurons. The somatosensory receptive fields of trimodal neurons are, on average, significantly larger than those of bimodal neurons, which, in turn, are substantially larger than those of unimodal neurons. This same relationship has been documented in the visual receptive fields of unimodal and multisensory superior colliculus neurons (Meredith and Stein, '90). Since behaving animals can displace their body and limbs without moving their eyes or head, it is possible to misalign the somatosensory and visual, or auditory, receptive fields. Thus for multisensory neurons, the larger these fields are the less likely that small movements will pull them out of register with one another. Additional evidence for this hypothesis is found in animals that are incapable of independentmovement of their different peripheral sensory organs, as in the barn owl, where auditory and visual receptive fields are substantially smaller (and in closer spatial register; Knudsen, '82) than those found in cats (Middlebrooksand Knudsen, '84; Meredith and Stein, '86a, '90) and guinea pigs (King and Palmer, '85).This is an important consideration, because the registry of different receptive fields is a critical determinant of multisensory integration (Meredith and Stein, '86a), which, in turn, influences overt behaviors (Stein et al., '89). The mechanisms by which multisensory superior colliculus neurons tend to obtain large receptive fields and unimodal neurons acquire smaller ones have yet to be determined. However, somatosensoryneurons with large or small receptive fields may have different functional roles by virtue of their efferent connections. Of the somatosensory neurons projecting to the contralateral brainstem and spinal cord, the vast majority (98%)are multisensory (Meredith et al., in press) and generally have large receptive fields. In contrast, whereas unimodal somatosensory neurons (i.e.,

usually with small receptive fields) are routinely found in the deep layers, disproportionately few (2%) send their s o n s into the tecto-reticulo-spinaltract (Meredith et al., in press). This dichotomy suggests that whereas somatosensory information generally derived from large receptive fields (i.e., multisensory neurons) is relayed to premotor regions to influence orientation behavior, that from smaller receptive fields (ie., unimodal neurons) has a different, as yet undetermined destination and function.

Resolution The large receptive fields of deep layer somatosensory neurons and the broad, overlappingrepresentational zones (i.e., dermal images) they constitute suggest that the somatotopy in the superior colliculus might lack the precision necessary for accurate localization of cutaneous stimuli. For example, neurons representing the forelimb have a distribution that is essentially coextensive with those that represent the face, a situation that renders localization impossible if this function is based solely on the distribution of relevant neurons. However, the neurons are not evenly distributed within a given dermal image but are concentrated in specificregions of the superior colliculus according to the different portions of the body represented-an arrangement that creates representational foci (i.e., best dermal images) of different body parts. This not only gives rise to the somatotopy, but also provides the substrate for the localization of cutaneous stimuli on the basis of the differential distribution of activated neurons within the superior colliculus. Given the considerable overlap among some of the best dermal images, however, their differential distribution is likely to provide the means for only comparatively coarse localization. The differential distribution of best dermal images need not be the only factor supporting localization €unctions in the superior colliculus. If a given stimulus evokes different levels of activity in the relevant pool of neurons and this

367

SOMATOTOPY IN DEEP SUPERIOR COLLICULUS

Multisensory

’

0

Multisensorv

Unimodal

U nimodal

0

----Best

Dermal Image o Dermal Image

Fig. 11. The relationship of recording penetrations with multisensory and unimodal somatosensory neurons to the dermal (dashed line)

and best dermal (solid line) images for the different body regions. Filled squares represent penetrations in which best dermal image criteria are met ( 2 75% neurons/penetration); open circles indicate penetrations

activity gradient is differentially distributed across the best dermal image, a considerably greater degree of resolution is possible. Recently it has been shown that somatosensory receptive fields of superior colliculus neurons are characterized by internal heterogeneities, where “best areas,” in which the thresholds for activation are lowest and activity evoked by equivalent stimuli is highest (Clemo and Stein, in press), are bordered by regions of progressively lower

that fulfilled criteria for dermal images. Each dermal and best dermal image is dominated by multisensory neurons, but note that multisensory and unimodal somatosensory neurons contribute to the generation of the same somatotopy.

sensitivity. Since these best areas occupy only a portion of the receptive field, a stimulus on the forepaw, for example, might fall within the best areas of receptive fields of only a portion of the neurons representing that cutaneous region and in none of best areas of those representing more proximal regions of the forelimb. In this case, even though neurons constituting both the best dermal images of the forepaw and the forelimb will be active, there will be a focus

M.A. MEREDITH ET AL.

368

Multisensory Neurons SC Location

Fig. 12. The somatosensory and visual receptive fields of multisensory neurons are in spatial register, as shown by these examples from one animal. A neuron in the rostral superior colliculus (left) has a somatosensory receptive field (right) on the face and a visual receptive field (far right) at the projection of the area centralis. Similarly, lateral and caudal neurons (left) have somatosensory receptive fields (right) on

the forepaw and hindlimb, whereas their visual receptive fields are in inferior temporal and inferior visual space, respectively (far right). These and other examples demonstrate that multisensory neurons contribute to the construction of both the somatosensory and the visual deep layer maps.

of highly active neurons within a subregion of the representation of the forepaw. Thus it is possible to derive activitydependent distinctions among the representations of adjacent body regions or even among neighboring points on the body surface, thereby enhancing the accuracy of localizing a cutaneous stimulus.

colliculus map. Despite the differing roles of the superior colliculus, lemniscal and spinothalamic systems and various somatosensory cortices, they all appear to require the same distortions in their representations of the body surface: magnification of the face and forelimb and constriction of the trunk, hindlimb, and tail.

Magnification

Somatotopy: One component of a multisensory map

In contrast to the distinctively large receptive fields and the multisensory nature of most somatosensory superior colliculus neurons, the somatotopic map revealed by the different best dermal images has the differential magnification of the face (especially areas around the mouth) and forepaw characteristic of the lemniscal, spinothalamic, and primary cortical systems. The face, which occupies a small cutaneous area (Z.6%),involves nearly 10times that proportion of the superior colliculus and, similarly, the forepaw accounts for 1.4%of the body surface but 27% of the map. Conversely, the trunk and hindquarters occupy large cutaneous regions but span only minor portions of the superior

The organization of sensory systems into maplike representations is common throughout the central nervous system. The trend is to segregate different representations so that a given nucleus or area of tissue is modality-specific. However, this is clearly not the plan in the deep layers of the superior colliculus, where visual, somatosensory, nociceptive (in rodents), auditory, and multisensory neurons are intermixed (e.g., Stein and Arigbede, '72; Gordon, '73; Drager and Hubel, '75, '76; Stein et al., '76; Tiao and Blakemore, '76; Chalupa and Rhoades, '77; Finlay et al., '78; Stein and Dixon, '78; Graham et al., '81; Rhoades, '81;

369

SOMATOTOPY IN DEEP SUPERIOR COLLICULUS T

S only

V only

SV Receptive fields / Visu6i

I

z

/

Fig. 13. Somatosensory responses can be dramatically influenced by the presence of nonsomatosensory stimuli. A somatosensory stimulus (ramp labeled “S”)reliably activated this neuron on most trials (7/8), as indicated by the raster (each dot = 1impulse) and peristimulus-time histogram (10 ms/bin). Similarly, a visual stimulus (ramp labeled “V”) also evoked a response on most trials (7iS). However, even though the different stimuli were effective individually, combining the two stimuli

(“SV”)produced a profound increase (290%)in the number of impulses and in the duration of the response on each presentation. These results are summarized in the bar graph to the right. The somatosensory and visual receptive fields of this bimodal neuron are shown at the bottom, where the arrowhead represents the location of the somatosensory stimulus and the bar and arrow indicate the location and vector of the visual stimulus, respectively.

Meredith and Stein, ’86a,b). Each sensory modality has a sponses in superior colliculus neurons that effect approprimaplike organization and is in general register with the ately directed attentive and orientation behaviors. others. The spatial correspondence among modalities is most obvious when comparing the different receptive fields of individual multisensory neurons. This representational ACKNOWLEDGMENTS plan, which differs so strikingly from that found in the The authors thank J. Nelson and N. London for their primary projection nuclei, is a reflection of the involvement of all of these sensory systems in the behavioral roles of the technical assistance. This work was supported by Grants superior colliculus. The deep superior colliculus does not NS-22543 and BNS 8719234. separate these different sensory representations because its job is one of providing the different modalities access to a LITERATURE CITED common circuitry. The majority of the somatosensory-responsive neurons Baleydier, C., and F. Mauguiere (1978) Projections of the ascending somesthetic pathways to the cat superior colliculus visualized by the horseradencountered here and in previous studies (Meredith and ish peroxidase technique. Exp. Brain Res. 31:43-50. Stein, ’86b) were multisensory. Furthermore, since every body region was primarily represented by multisensory Berkley, K.J., A. Blomqvist, A. Pelt, and R. Flink (1980) Differences in the collateralizationof neuronal projections from the dorsal column nuclei neurons, it was the multisensory neurons that formed the and lateral cervical nucleus to the thalamus and tectum in the cat: An major component of the somatotopic map. These somatosenanatomical study using two different double-labeling techniques. Brain Res. 202.273-290. sory-responsive neurons are subject to strong influences from other sensory modalities (Meredith and Stein, ’86a,b; Blomqvist, A,, R. Flink, D. Bowsher, S . Griph, and J. Westman (1978) Tectal and thalamic projections of dorsal column and lateral cervical nuclei: A Meredith et al., ’871, and it may be inappropriate to think of quantitative study in the cat. Brain Res. 141:335-341. these neurons, or this map, as equivalent to those in Chalupa, L.M., and R.W. Rhoades (1977) Responses of visual, somatosensory unimodal somatosensory areas of the brain. Rather, it is and auditory neurons in the golden hamster’s superior colliculus. J. but one component of an integrated, multisensory represenPhysiol. (Lond.)270:595-626. tation. This arrangement ensures that cues from different Clemo, H.R., and B.E. Stein (1984) Topographic organizationof somatosensory corticotectal influences in cat. J. Neurophysiol. 5k843-858. sensory modalities, or their combinations, trigger re-

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M.A. MEREDITH ET AL. of multisensory neurons in cat superior colliculus. Brain Res. 365350354. Meredith, M.A., and B.E. Stein (198613)Visual, auditory and somatosensory convergence on cells in superior colliculus results in multisensory integration. J. Neurophysiol. 56:640-662. Meredith, M.A., and B.E. Stein (1990) Visuotopic component of the multisensory map in the deep layers of the cat superior colliculus. J. Neurosci. 1Ot3727-3742. Meredith, M.A., H.R. Clemo, and B.E. Stein (1990) Somatotopic component of the multisensory map in the deep layers of the cat superior colliculus. SOC. Neurosci. Abstr. 16r223. Meredith, M.A., J.W. Nemitz, and B.E. Stein (1987) Determinants of multisensory integration in superior colliculus neurons: I. Temporal factors. J. Neurosci. 7:3213-3229. Meredith, M.A., M.T. Wallace, and B.E. Stein (1991) Visual, auditory and somatosensory convergence in output neurons of the cat superior colliculus: Multisensory properties of the tecto-reticulo-spinal projection. Exp. Brain Res. (in press). Middlebrooks, J.C., and E.I. Knudsen (1984) A neural code for auditory space in the cat’s superior colliculus. J. Neurosci. 4:2621-2634. Moschovakis, A.K., and A.B. Karabelas (1985) Observations on the somatodendritic morphologv and axonal trajectory of intracellularly HRPlabeled efferent neurons located in the deeper layers of the superior colliculus of the cat. J. Comp. Neurol. 239.276-308. Nagata, T., and L. Kruger (1979) Tactile neurons of the superior colliculus of the cat: Input and physiological properties. Brain Res. 174: 19-37. Ogasawara, K. (1981) Trigeminotectal projections in cats and the pathway of extraocular proprioception. J. Neuro-ophthalmol. 1:219-230. Ogasawara, K., and K. Kawamura (1982) Cells of origin and terminations of the trigeminotectal projection in the cat as demonstrated with the horseradish peroxidase and autoradiographic methods. Okajamas Folia Anat. Jpn. 58247-264. Rhoades, R.W. (1981) Cortical and spinal somatosensory input to the superior colliculus in the golden hamster: An anatomical and electrophysiological study. J.Comp. Neurol. 195:415432. Stein, B.E. (1984) Multimodal representation in the superior colliculus and optic tectum. In H. Vanegas (ed): Comparative Neurology of the Optic Tectum. New York: Plenum, pp. 819-841. Stein, B.E., and M.8. Arigbede (1972) Unimodal and multimodal response properties of neurons in the cat’s superior colliculus. Exp. Neurol. 36:179-196. Stein, B.E., and J.P. Dixon (1978) Properties of superior colliculus neurons in golden hamster. J. Comp. Neurol. 183r269-284. Stein, B.E., and N. Gaither (1981) Sensory representation in reptilian optic tectum: Some comparisons with mammals. J. Comp. Neurol. 202r69-87. Stein, B.E., B. Magalhaes-Castro, and L. Kruger (1976) Relationship between visual and tactile representation in cat superior colliculus. J. Neurophysiol. 39r401-419. Stein, B.E., R.F. Spencer, and S.B. Edwards (1983) Corticotectal and corticothalamic efferent projections of SIV somatosensory cortex in cat. J. Neurophysiol. 50:896-909. Tiao, Y.-C., and C. Blakemore (1976) Functional organization in the superior colliculus of the golden hamster. J. Comp. Neurol. 168t483-506.