Experimental Brain Research

Exp. Brain Res. 34, 299-320 (1979)

@ Springer-Verlag 1979

I. Functional Properties of Neurons in Lateral Part of Associative Area 7 in Awake Monkeys L. Leinonen, J. Hyv/irinen, G. Nyman, and I. Linnankoski Institute of Physiology,University of Helsinki, Siltavuorenpenger20 J, SF - 00170 Helsinki 17, Finland

Summary. The lateral part of area 7, area 7b, of alert, behaving macaque monkeys was investigated using transdural microelectrode recording technique. Two hundred twenty-eight cells from five hemispheres of four monkeys were isolated and studied. The functional properties of 2 % of the cells isolated remained unidentified. Functions of the identified cells were prominently related to the spatial control of arm movements. Of the cells 70 % responded to somatosensory (40 %) or visual (16 %) or both somatosensory and visual (14%) stimulation. The receptive fields of these passively drivable cells were large, covering, e.g., the arm or leg or chest or even the skin of the whole body. Most of the visually drivable cells responded to stimuli in both halves of the visual field. Of the cells responding to sensory stimulation 80 % were activated by stimuli moving in a certain direction. Of the directionally selective cells 25 % received information through more than one sensory channel. The complex stimulus-response relationships of these "convergence" cells revealed the existence of an integrative system which analyzes the direction of a stimulus moving in one sensory system using an other sensory system as a reference. Of all the cells isolated 28 % discharged only during active movements of the arms (25~ or eyes (3 %). Firing of these neurons was related to contraction of a functionally uniform group of muscles and not individual muscles. Some previous investigations of the parietal association cortex, conducted mainly in area 7a, have shown that most cells are active only when the monkey himself moves his eyes or arms. In our study on area 7b most cells responded to passive stimulation. The discrepancy between the results indicates functional differentiation within area 7. Key words: Parietal lobe - Association cortex - Microelectrode recording Monkey - Behavior Offprint requests to: L. Leinonen, M.D. (address see above)

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L 20

Fig. 1. The sulci of the parietal lobe and the recording site of the present work (hatched). The stereotaxic planes AP 0 and L 20 are indicated at the margins

One of the main symptoms caused by posterior parietal lesions in man (lesion in area 7, 39, or 40 of Brodmann) and monkey (lesion in area 7) is the defect in spatial control of movements and in analysis of spatial relationships both of somesthetic and visual stimuli. In man this is revealed, for instance, in difficulties in manual construction and somesthetic recognition of objects; estimation of distances and visuospatial relations; route finding and using of maps (review articles by Critchley, 1953; Denny-Brown and Chambers, 1958), and in monkey, e.g., in disturbances in tactile discrimination of roughness or shape (Ruch et al., 1938; Ettlinger and Kalsbeck, 1962); manual reaching and grasping (Peele, 1944; Semmes Blum et al., 1950; Bates and Ettlinger, 1960; Ettlinger and Kalsbeck, 1962); estimation of distances and visuospatial relations (Pohl, 1973; Ungerleider and Brody, 1977). Furthermore, clinical studies in man have revealed that lesions in different parts of the parietal association cortex result in different symptoms. This suggests that there is functional differentiation within this area. Although area 7 of the monkey has been studied with microelectrode recording technique during recent years by several investigators (Hyv~irinen and Poranen, 1974; Mountcastle et al., 1975; Lynch et al., 1977; Yin and Mountcastle, 1977; Robinson et al., 1978), functions related to intersensory spatial analysis, revealed by ablation studies, were reported only by Hyv~irinen and Poranen. No regional differentiation within area 7 of the monkey has been described so far. We investigated with microelectrode recording technique the lateral part of area 7, termed 7b (Vogt and Vogt, 1919) or PF (von Bonin and Bailey, 1947) (Fig. 1), trying to answer the two questions raised by the findings of ablation studies: 1. How does the activity of single cells reflect the intersensory analysis

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o f s p a t i a l r e l a t i o n s h i p s ? 2. Is t h e r e a n y f u n c t i o n a l d i f f e r e n t i a t i o n w i t h i n a r e a 7 ? For each cell isolated we determined what factors in the monkey's surroundings o r i n its o w n b e h a v i o r w e r e r e l a t e d t o c h a n g e s i n c e l l u l a r a c t i v i t y . A w i d e s c a l e o f qualitatively different stimuli were used to get comprehensive and unbiased information of cellular functions.

Materials and Methods Four hemispheres of 3 female stump-tailed monkeys (Macaca speciosa) weighing 7 to 8 kg were studied. The recording techniques have been described in detail by Hyv~irinen and Poranen (1974). Extracellular recordings were made using glass coated tungsten microelectrodes (tip length 15-20 [xm, diameter 8-10 p.m). A modification of the procedure of Levick (1972) was used in the preparation of the electrodes. An Evarts hydraulic mieromanipulator was used for transdurat penetrations (Evarts, 1966). During the experiments the monkey's head was immobilized by a firm halo fixation device (Friendlich, 1973). Horizontal and vertical eye movements were monitored with Ag/AgC12 electrodes implanted into the skull around the orbits (Bond and Ho, 1970). Cellular activity, eleetro-oculograms, verbal description of the stimuli and their manually triggered timing pulses were stored on tape with an 8-channel tape recorder (Precision Instrument Company, PI-6200). Some recordings were photographed with a polaroid camera from a storage oscilloscope (Tektronix, Inc., 5103N). Recordings took place in a dimly lit laboratory room where the monkey sat in a primate chair in which it could move its limbs when desired. No fluid or food deprivation preceded the experiments. The monkeys were offered juice, raisins, and pieces of banana to direct their attention and keep them docile. A good relationship between the monkey and the investigators was established before the experiments by handling and feeding the monkey daily. In the course of the experiments a nervous monkey could be calmed, for instance, by grooming it. To reduce the risk of infections during the experiments, the monkey was given tetracycline perorally and the dura and the wound were kept clean with iodine detergent. Recordings in one hemisphere continued for 2 to 12 weeks. A recording session lasted 4 to 6 h after which the monkey was released to its cage. All cells were investigated with numerous stimuli even after one effective stimulus was found. All cells were routinely examined by touching various parts of the body, palpating and rotating the limbs and the body; by various visual and auditory stimuli and by letting the monkey reach for a raisin, a piece of banana, or some other object with its hand (reaching with foot in the recording chair was possible only without visual guidance), and by letting it bite hard and soft objects. An active flexion of the arm was resisted by the examiner in order to discover if isometric contraction of arm muscles was related to the cellular activity. At the beginning of the recordings in each monkey, the cortical area covered by the microdrive cylinder was mapped using electrodes with 100 ~m long and 30 ~tm wide tips. In this way, the locations of the intraparietal sulcus and the Sylvian fissure could be determined. Using microdrive coordinates of the sulci it was possible to concentrate the penetrations on the lateral part of area 7. All penetrations near the Sylvian fissure that reached its medial wall (penetrations in which the activity continued longer than the normal thickness of the cortex warranted) were excluded from this material. Some penetrations reached the medial border of the Sylvian fissure several millimetres deep; the activity obtained from the Sylvian fissure was excluded from the material. No penetrations were made lateral and anterior to the anterior end of the intraparietal sulcus. Penetrations made into the anterior border of the intraparietal sulcus were excluded from this study. Three monkeys were killed after the recording period. Using the coordinates of the microdrive map several points of the cortex were marked by insertion of electrodes into the brain with the Evarts microdrive. The guiding electrodes were left in the brain which was put in formalin. The penetrations included in this material were then localized using the guiding electrodes and the microdrive map. The macroscopical identification of the location of the recording site yielded essentially the same results as did the functional mapping technique. The parietal cortex was studied histologically in three brains to identify the anterolateral margins of area 7. Because of the long recording periods and the great number of penetrations, individual electrode tracks were not marked with electrocoagulation and could therefore not be identified in the histological investigation. Comparison of the results from the

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macroscopical localization and histological investigation verified that the whole area recorded was within area 7 (cytoarchitectural criteria of yon Bonin and Bailey, 1947). The area recorded was posterior to the cytoarchitecturally distinct vestibular projection field in area 2 which lies within and around the lateral wall of the anterior end of the intraparietal sulcus. This area has been investigated by Schwarz and Fredrickson (1971). According to functional criteria given by Woolsey (1958, personal communication 1977) area S II is posterior to the anterior end of the intraparietal sulcus completely embedded in the Sylvian fissure. All cells isolated within the Sylvian fissure or near it were excluded from the study.

Results The cells described in this work were isolated from an area of 6 x 8 mm (Fig. 1). Two hundred twenty-eight cells were isolated and studied. Five of them (2 %) could not be excited by any of the stimuli used nor was there any noticeable correlation between the cellular activity and the monkey's behavior. The cells were classified according to their responsiveness to stimulation of different receptors or according to the type of behavior which correlated with the cellular activity (Table 1). The classes of cells in Table 1 are reviewed separately below and examples of responses of neurons in different classes are given.

Table 1. Classification of the cells according to their responsiveness to stimulation of different receptors or according to the type of behavior which correlated with the cellular activity Number of cells Cells responding to sensory stimulation I Somatosensory a. Skin b. Joint c. Muscle or tendon d. Skin and muscle II Visual a. Any moving object b. Meaningful object III Somatosensory and visual/oculomotor a. Skin and visual b. Joint and visual/oculomotor c. Skin and muscle/joint and visual/oculomotor Cells active only during intentional movements IV Somatic a. Reaching b. Manipulation c. Other movements of fingers, hand, arm or shoulder V Ocular VI Not identified Total

%

159 91 28 8 45 10 36 20 16 32 20 3 9

70 40 12 4 20 4 16 9 7 14 9 1 4

64 57 24 10 23

28 25 11 4 10

7

3

5

2

228

100

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Fig. 2. Receptive fields (hatched) of all the cells that responded only to cutaneous stimulation. For simplicity, the right side of all the monkeys presents the side contralateral to the hemisphere recorded. Short arrows near the receptive fields indicate that the receptive field covers also the backside of the limb or the body. Arrows on the receptive fields (cells no. 22-28) indicate the direction in which the stimuli had to move to be effective. One neuron responded to stimuli moving in any direction (cell no. 2)

O n e h u n d r e d eighteen cells ( 5 2 % ) r e s p o n d e d exclusively to one o f the following stimuli: exteroceptive, proprioceptive or visual. F o r 41 cells ( 1 8 % ) two or three o f these types of stimuli were effective. Sixty-four cells ( 2 8 % ) discharged only during certain m o v e m e n t s executed by the m o n k e y .

Cells Responding to Somatosensory Stimulation Cells R e s p o n d i n g to C u t a n e o u s Stimuli Cells responding to touching of the skin usually had quite large receptive fields which typically c o v e r e d entire parts o f the b o d y such as the hands or arms (12 cells), chest, neck a n d / o r face (5 cells), back (3 cells), feet or legs (5 cells). S o m e cells had extremely extensive receptive fields: all the skin a b o v e the navel (2

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]Fig. 3. A Cutaneous receptive field of a directionally selective cell. Arrows indicate the direction of movement of effective stimuli. B The mean firing rates (and the standard deviations) of the cell as a function of the speed of the stimulus movement. The stimulus, light stroking with a finger along the skin from the elbow to the fingertips, was repeated 5 times at each speed

cells), the whole skin of the body with the exception of a zone around the waist (1 cell). The receptive fields of the cells in this group are illustrated in Fig. 2. Twenty cells were responsive to light touching of the skin or the hair. The responses were normally transient and diminished on repetitive stimulation. Two of these neurons did not respond with excitation to any of the stimuli used (the only cells in this study besides the unidentified cells). Their spontaneous activity was tonically inhibited by touching the contralateral forefinger and foot. The spontaneous firing rate of these neurons was higher than that of any of the cells with excitatory responses. Eight of the cutaneously drivable cells (Fig. 2: Nos. 2, 2 2 - 2 8 ) were sensitive to stimuli moving along the skin. Three cells in the left hemisphere discharged only when the stimulus m o v e d from right to left on the chest but were unresponsive to m o v e m e n t from left to right, upwards or downwards (Fig. 2: Nos. 22-24). Three cells responded selectively to m o v e m e n t from proximal to distal; their receptive fields covered the skin of the body above the navel or the entire skin of the body except a 15 cm-wide zone around the waist (Fig. 2: Nos. 25, 26, 28). On the upper trunk the effective direction was towards the head and on the head towards the mouth.

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Figure 3 illustrates properties of a cell which responded to all moving skin stimuli on the trunk above the navel and on the head towards the mouth and on the upper limbs towards their distal ends. Within limits the frequency of the firing increased as the speed of the movements increased. The cell had no spontaneous activity.

Cells Responding to Stimulation of Joints Six cells responded to rotation of one joint (i.e., shoulder, wrist). Two cells were excited by rotation of several joints; i.e., flexion of the wrist and finger joints; flexion of the wrist, elbow, and rotation of the shoulder joint. On repeated stimulation the cells did not habituate markedly.

Cells Responding to Stimulation of Muscles or Tendons Fourty-five cells fired during palpation and stretching of muscles (stretching was induced by rapid or forced rotation of joints). Those neurons that fired during slow extension or flexion from any position of the joint were classified as "responding to stimulation of joints" whereas the ones responding only to very rapid movement of the joint or to extreme (forced) extension or flexion were classified as "responsive to stimulation of muscles or tendons". Most of the cells that responded to stimulation of muscles discharged when the muscles moving the wrist or fingers were stimulated. Only five cells responded to palpation of the legs or back; four cells responded to stimulation of the shoulder, chest or face. Usually stimulation of a group of muscles (e.g., flexors of the elbow or wrist, flexors of individual fingers or all fingers) activated the cell. As a rule the cells discharged also during active contraction of the muscles.

Cells Responding to Stimulation of the Skin and Muscles This group consisted of ten cells which were activated by palpation of muscles and by light touching of the skin above the muscles or in their vicinity. Five of them responded both to palpation of the flexors of the wrist and fingers and to light touching of the fingertips.

Cells Responding to Visual Stimuli

Cells Responding to Any Moving Visual Stimuli This group consisted of twenty cells that responded to any moving visual objects (white sheet of cardboard, experimenter's hand, other objects of various sizes). Three cells were activated maximally by stimuli moving towards (2 cells) or

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away (1 cell) from the animal. Ten cells responded only to stimuli moving in one of the following directions: from left to right, upwards, downwards. For three cells the direction of movement was not crucial. Receptive fields were usually large, one or both halves of the visual field. This was tested by presenting the stimuli in different parts of the visual field while the monkey was fixating an interesting object directly in the front of him. However, four cells discharged only when the object was moving in the periphery of the visual field. The maximal response was triggered by an object which unexpectedly moved from the border into the visual field. If this stimulus was presented many times in succession or if the monkey's attention was drawn elsewhere by an interesting object, the response diminished or disappeared.

Visually Drivable Cells Responding to Other Stimulus Properties Than Direction or Speed of the Movement Eleven cells responded transiently to interesting stimuli, e.g., a banana, raisin, or merely a novel object. These stimuli almost always triggered visual fixation. After repetitive or prolonged presentations of the same object, fixation no longer resulted in a cellular response. Thus, the cellular activity was related to the interest that the object evoked in the monkey. Three neurons fired maximally when the animal was rotating and looking at its hand. Responses could not be obtained by rotating the hand passively while the monkey was watching it. Nor did any other visual stimuli used activate these cells. One cell fired when the experimenter's hand approached a package of raisins. The cell 9stopped responding if the animal was not given a raisin after several stimuli (hand approaching package). The distance between the monkey and the triggering visual stimulus, whether stationary or moving, was crucial for the response. Most cells did not respond when the stimulus was at a distance of more than 1 m from the monkey. The effect of distance could not be compensated a t longer distances by increasing the size of the stationary object or by increasing the velocity of the movement.

Cells Responding Both to Somatosensory and Visual Stimulation Cells Responding to Cutaneous and Visual Stimulation This group consisted of 20 cells. The cutaneous receptive fields of these neurons covered the arm(s) or a part of an arm (15 cells), chest (3 cells), arm and chest (1 cell) or chest and face (1 cell). Seventeen cells responded both to light touching of the skin and to visual stimuli which moved towards the cutaneous receptive field from the distance of about 30 cm or were near it, at the distance of 5-10 cm. When the cutaneous receptive field was on the arm, responses to approaching visual stimuli were verified also in different positions of the arm. Responses to cutaneous stimuli

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Fig. 4. A-G. Activity of a cell which responded to touching of the contralateral arm and to visual

stimuli approaching or near the contralateral arm. The trace below the cellular activity shows the horizontal EOG; positive deflections indicate eye movements in contralateral direction. The monkey's eyes are covered in A, B, and C. A Touching of the ipsilateral arm (--). B Touching of the contralateral arm (--). t2 Fifth successive touching of the receptive field (--). D Experimenter's hand approaches the contralateral arm (--) from the contralateral side and stays above it (. . . . ). E Experimenter's hand approaches the ipsilateral arm (--) from the midline and is then moved immediately away. F, G Experimenter's hand approaches from the midline the contralateral arm (--)

were triggered also w h e n the m o n k e y ' s eyes were covered. T h e cells did usually n o t r e s p o n d to blowing of the hair. Figure 4 presents some responses o f this type o f cell. T h e n e u r o n h a d a slow s p o n t a n e o u s activity. It had a cutaneous receptive field o n the contralateral arm. A light touching of the receptive field resulted in tonic discharge if the m o n k e y could see the t o u c h i n g object, and in an o n - o f f response w h e n the m o n k e y ' s eyes were c o v e r e d (Fig. 4B, C). The response diminished on repetitive t o u c h i n g (Fig. 4B c o m p a r e d to 4C). The cell also r e s p o n d e d w h e n the e x p e r i m e n t e r ' s h a n d (or an object in the e x p e r i m e n t e r ' s h a n d ) a p p r o a c h e d the contralateral arm f r o m any direction (Fig. 4D, F, G) or stayed n e a r it (Fig. 4D). The m o n k e y was watching these stimuli all the time. T h e examination o f the horizontal (in the figure) and the vertical eye m o v e m e n t s revealed that the response was not d e p e n d e n t on the direction of the gaze per se. F o r comparison, the figure also shows cellular activity during

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~ 0.5S Fig. 5. A-F. Responses of a cell to moving cutaneous and visual stimuli. In A, eyes covered, the monkey's chest is stroked with a finger from right to left and in B from left to right. In C and D eyes open, the stimuli are the same as in A and B. In E a visual stimulus (the investigator's hand) moves from right to left at a distanee of 15 cm from the chest and in F from left to right approaching stimuli towards the ipsilateral arm. These stimuli as well as m o v e m e n t s approaching other parts of the body were not effective. In most cases when a cell responded to visual stimuli approaching the cutaneous receptive field both the cutaneous receptive field and the approaching visual stimulus could be seen by the m o n k e y simultaneously. However, even when the cutaneous receptive field could not be seen by the m o n k e y (e,g., the receptive fields on the chest could not be seen because of the head fixation) only stimuli approaching the receptive field evoked a response. This indicates that the direction of m o v e m e n t was not in reference to the location of the projection of the referred skin area on the retina but rather to the relative position of the cutaneous receptive field in the somesthetic system. Thus, it can be inferred that these cells received proprioceptive information (which, however, is not revealed in the classification of these cells). The responses to approaching visual stimuli were constant, and they did not correlate with any specific muscle contraction. Therefore, they were probably not related to preparatory muscle tension which might follow an approaching visual stimulus. It was sometimes noticed, but not systematically examined, that cells that had their receptive fields on the hand became active when the m o n k e y ' s hand came near the object it was reaching for. Covering one of the m o n k e y ' s eyes did not affect responses of these cells to approaching visual stimuli including those moving in the depth dimension towards the cutaneous receptive field on the face or chest. One cell was excited by light touching of the arm and by visual stimuli moving in any direction. Two cells responded both to light stroking across the chest from right (the contralateral side) to left and to visual stimuli moving towards the chest or near it (within 50 cm) in a direction parallel to the optimal

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0.5S Fig. 6. A-D. Activityof a cell, A during a visual stimulus (a spot of light on a screen) moving from right to left in the visual field, B during a visual stimulus moving in reversed d~rection, C (eyes covered) during passive movement of the ipsilateral (right) arm from right to left (hand movement towards the sagittal plane was caused by rotation of the shoulder joint and flexion of the elbow), and D during reversed movement of the arm

cutaneous stimulus. Figure 5 presents responses of a cell activated by light stroking across the chest and shoulders from right to left and by visual stimuli moving in the same direction near (within 20 cm) the chest. When the monkey was sitting still with its eyes closed, the spontaneous firing rate of this cell was very low. It increased up to 3-6 spikes/s when the monkey opened its eyes.

Cells Responding to Visual Stimulation and Passive Joint Movement Two cells were active both during visual tracking and passive joint rotation. The responses to joint movements were independent of vision (responses were not affected by covering the eyes) or eye movements. One of these cells discharged during tracking eye movements downwards or when the monkey's arm was moved in the same direction either from the elbow or shoulder joint or both. The other cell discharged during tracking eye movements from the ipsilateral to the contralateral side and during supination of the contralateral shoulder joint. One neuron was activated by visual stimuli moving from right (the ipsilateral side) to left and by passive movements of either arm in this same direction (Fig. 6). The effective movement in the contralateral arm was caused by slight supination of the shoulder joint and extension of the elbow joint; in the ipsilateral arm, by slight pronation of the shoulder joint and flexion of the elbow joint. This cell was not activated by pronation or supination of the shoulder joint or by flexion of the elbow in such position of the shoulder joint in which the hand moved in the upward direction. When the monkey was sitting still, eyes closed, the cell did not discharge.

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Cells Responding to Exteroceptive, Proprioceptive and Visual Stimuli Nine cells received input from both exteroceptors, proprioceptors, and retina. Eight of them responded only to cutaneous and visual stimuli moving in a certain direction; when the monkey was sitting upright the objective direction of the effective cutaneous and effective visual stimulus was the same. Four of these cells responded also to such passive movements of joints which caused a limb or a part of it to move in the same direction as the effective cutaneous and visuat stimuli, for example: When the monkey was sitting upright the cell responded to visual stimuli moving both from right to left and downwards in the visual field. The cell responded also to blowing on the fur of the chest from the right (but not from the left) and to cutaneous stimuli moving from right to left on the chest, face and palmar side of the hand. A cutaneous stimulus moving on the palm was effective only if the hand was in such a position that the stimulus moved from right to left (in reference to body axis and visual field). Thus, all directions of movement on the skin were potentially effective. The cell was activated also by movement of the upper or lower arm from right to left caused by passive flexion/extension of the elbow joint and rotation of the shoulder joint. When the head was tilted about 90 ~ to the left, visual stimuli moving from right to left (in reference to the body axis, not the head) did not activate these cells, whereas movement from right to left in the visual field was now effective. Tilting of the head did not affect the responses to cutaneous stimuli on the chest or face, e.g., the direction (in reference to the skin) of the effective cutaneous stimulus did not change when the visual field was rotated. We could not study if this was also true for passive joint movements and cutaneous stimuli on the palms. Effective stimuli for a similar cell are illustrated in Fig. 7, No. 6; Nos. 1-5 illustrate effective stimuti for cells which responded also to other kind of stimuli than those moving in a certain direction. The responses to somesthetic stimuli were always examined also when the monkey's eyes were closed; covering of the eyes did not influence the responses.

Cells Discharging Only During Active Movements of Limbs Cells Active During Reaching with Hand Twenty-four cells discharged just before and during extensive movements of the arms which were ment for grasping an object. The activity of these cells ceased when the monkey touched the object, although the extension of the arm still prevailed. This supported the idea that the cellular activity correlated with the conditioned reaching response rather than with the extensive arm movement in general. The triggering stimulus could be food or other interesting objects. Because of lack of the monkey's cooperation only some of these cells could be examined with the monkey's eyes covered during reaching. Excluding the vision did not influence the activity of these cells. Figure 8 presents responses of a cell which was active during reaching with either arm or either side of the mouth. In the figure, the two bursts of activity

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Fig. 7. Characteristics of the effective stimuli for 6 neurons. All of them responded to moving visual stimuli. The arrows above the monkeys indicate the directions in which moving stimuli were effective. Three cells responded also to visual stimuli approaching the hands or the chest as indicated in the figure. All the cells had cutaneous receptive fields (hatched). Five ceils responded only to stimuli moving in a certain direction (indicated by the arrow on the receptive field). All the cells were activated also by palpation of muscles (indicated in the figure) or rotation of joints (indicated in the figure)

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0.2s Fig. 8. Cellular responses during the following behavioral sequence: 1. reaching with the arm for a raisin, 2. (indicated by the timing pulse) touching the raisin with the fingers, grasping it and bringing it towards the mouth, reaching with the lips for the raisin from the fingers, 3. touching the raisin with the lips and putting it into the mouth

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correspond to reaching with arm for a raisin and reaching with lips when the raisin is near the mouth. The activity ceased immediately when the m o n k e y touched the raisin with its hand or lips. When the m o n k e y was sitting still with no observable muscle contractions the cell started to fire as a strange (novel) object was m o v e d near its hand. When the m o n k e y lost interest in the approaching object, the response disappeared. This cell had no spontaneous activity. Cells Active During Manipulation Ten cells fired when the m o n k e y touched and manipulated a desired object. The activity of these cells was related to fast changes in the contraction of the flexors or extensors of the fingers. Figure 9 gives an example of a cell which was active during manipulation with fingers of either hand. The neuron had no spontaneous activity and could not be activated by passive palpation or moving of limbs. The activity during manipulation did not depend on the position of the wrist, elbow or shoulder joint; this was tested by making the m o n k e y reach for and manipulate a raisin from different directions. The activity of the cell, which was slow and monotonous, apparently did not reflect the dynamic and rapid changes in the sensory feedback and m o t o r control that take place during the manipulation. Cells Active During Other M o v e m e n t s Twenty-three cells were active only during grasping and bringing an object to the mouth. Many of them were selectively active during flexion of the fingers, flexion of the elbow or m o v e m e n t s of the shoulder joint. In some cases an increase in the force of isometric contraction was synchronous with the enhancement of cellular activity.

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Cells Active During Eye Movements The activity of 7 cells correlated only with eye movements: tracking (3 cells), convergence (2 cells), saccades (1 cell), steady fixation (1 cell). All cells whose activity correlated with eye movements were isolated inside or near the intraparietal sulcus.

Other Criteria for Classification "Laterality" of the Cells Table 2 presents a classification in which the cells are grouped according to the laterality of their receptive fields or body parts whose movement correlated with the cellular activity. The ceils were defined as bilateral if they were activated by stimulation on either side of the monkey (skin, joints, muscles, visual field) or if they discharged during the monkey's own movements of either side of the body. The cells active during eye movements were all defined as bilateral. Cells that could be activated bilaterally usually showed stronger responses to stimulation on the contralateral side.

Table 2. Laterality of the receptive fields and of the body parts whose movement correlated with the cellular activity. Contralateral = the side of the monkey which is contralaterally to the hemisphere recorded, ipsilateral = the side ipsilaterallyto the hemisphere recorded and bilateral = both sides of the monkey Number of cells

%

Contralateral Ipsilateral Bilateral

135 5 83

61 2 37

Total

223

100

Body Parts Related to the Activity of the Cells Of the cells that responded to somatosensory stimulation 70 % (86 of 123) had receptive fields on the arm(s) and 90% (57 of 64) of the cells that discharged only during the monkey's motor behavior were active during arm movements. These findings imply that our recording site was strongly related to receptive and motor functions of the arms. Moving Versus Stationary Stimuli Most (80 %) of the passively drivable cells responded to stimuli moving in a certain direction; 25 % of them received information through more than one

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sensory channel. It was often verified that when visual and somatosensory system were both involved, either of these systems was used as the frame of spatial reference. For instance, for 17 cells responding to touching of the skin and to visual stimuli approaching the cutaneous receptive field (but not to any other visual stimuli) the frame of reference for direction of moving visual stimuli was the somatosensory system. For 12 cells the frame of reference for direction of movement of a somatosensory stimulus was probably the visual (vestibular?) system. These neurons were activated by visual stimuli moving in a certain direction, by moving cutaneous stimuli, or passive limb movements in the same direction (referred to the visual field). Under restricted conditions the "convergence" cells responded only to such visual, proprioceptive and exteroceptive stimuli whose direction of movement were the same (parallel) in the objective world. Habituation Cells that responded to palpation or joint movement showed no marked habituation on repetitive stimulation. Some cells responsive to cutaneous or visual stimuli showed quick habituation if the interstimulus interval was short (usually less than half a minute). Six cells were activated only by novel (or unexpected) visual stimuli; after a few presentations of the same object the cells stopped responding. Influences of the Internal State of the Monkey When the animal got tired or inattentive, or when its attention was diverted from the stimulus, the response often decreased or disappeared. Presentation of food was an appropriate stimulus for some cells, the preferred food causing the maximal response. Sometimes the response to food stimuli disappeared when the monkey was made aggressive.

Discussion

Our Results in Light of Previous Studies Most cells (70%) investigated in the lateral part of area 7 responded to cutaneous, proprioceptive or visual stimulation. Receptive fields of these neurons were usually large, including, for instance, both halves of the visual field or the skin of entire parts of the body, e.g., hand, arm, shoulder, or chest. The passively drivable cells usually responded to stimuli moving in a certain direction; many of these cells received information through more than one sensory channel. Some of the cells (28%) were active only during the monkey's own movements, reaching with the arm, or lips, during exploratory behavior with fingers or lips or when the monkey was bringing an interesting object to the mouth. The results indicate that the lateral part of area 7 (area 7b of Vogt and

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Vogt or PF of von Bonin and Bailey) participates in intersensory analysis of spatial relations between moving stimuli and the monkey's own movements. Moreover, since most cellular functions were related to receptive or motor functions of the arms, we suggest that this area is specialized in spatial control of arm movements. Our results confirm the findings of other investigators who showed that: cells in area 7, in contrast to the primary sensory areas, have wide receptive fields (Hyv/irinen and Poranen, 1974; Yin and Mountcastle, 1977; Robinson et al., 1978); they receive information from several sensory organs (Hyv/irinen and Poranen, 1974; Mountcastle et al., 1975; Robinson et al., 1978); they discharge only during active arm or eye movements (Hyv/irinen and Poranen, 1974; Mountcastle et al., 1977); their activity is influenced by the monkey's emotional or motivational state (Hyv~irinen and Poranen, 1974; Mountcastle et al., 1975; Lynch et al., 1977). Our results differ from those of Mountcastle et al. (1975) and Lynch et al. (1977) in so far as the majority of their cells (80 %)were active only during the monkey's own movements, most during conditioned eye movements (fixation, tracking, saccades). This difference between the results is probably not due solely to different methods of testing. Mountcastle et al. and Lynch et al. investigated an area which is medial to our recording site and apparently mainly within area 7a. The discrepancy between the results may thus merely indicate functional differentiation within area 7. This is supported also by the following anatomical and physiological findings: 1. Histologically, area 7 is divisible into area 7a and 7b (Vogt and Vogt, 1919) or into PG and PF (von Bonin and Bailey, 1947); 2. The intrahemispheric connections of the medial part of area 7 (Ta) are different from those of the lateral part (Tb). The medial part sends fibers to the anterior side of the arcuate sulcus and to its medial parts including the frontal eye field whereas the lateral part sends fibers mainly to the caudal bank of the lateral arcuate sulcus (Pandya and Kuypers, 1969; Chavis and Pandya, 1976). The cortex within the concavity of the arcuate sulcus sends fibers to area 7a (Pandya and Kuypers, 1969). Thus, it seems propable that only area 7a has reciprocal connections with the frontal eye field. 3. Kaas et al. (1977) have reported that the efferent connections of the posterior parietal association cortex in the owl monkey terminate in several separate ipsilateral and contralateral foci within the posterior parietal cortex. They conclude: "Since both ipsilateral and callosal connections between heterotopic parts of the same area are uncommon and connections between different areas prevail, the separate ipsilateral and contralateral foci of terminations within the posterior parietal cortex argue that it is not a single area of the cortex". 4. Areas 7a and 7b respond in different ways to electrical stimulation. Vogt and Vogt (1919) found that stimulation of area 7a caused conjugate eye movements in the contralateral direction and stimulation of area 7b caused complex arm movements. Similar findings have been reported by Fleming and Crosby (1955) and by Lilly (1958). The method of testing of Mountcastle et al. and Lynch et al. was different from ours in so far as they observed cellular activity mainly during experimentally conditioned behavior. They used a set of standardized stimuli and taught the monkey to respond to some of them with a movement of the arms

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or eyes. This may account for certain differences in the results, e.g., the number of unidentified cells was higher in their investigations and the "convergence" neurons were rare. The aim of our study was to obtain data on the nature of the cellular functions in the lateral part of area 7 which has not been thoroughly studied with microelectrode technique. Due to the explorative nature of this investigation we did not teach the monkeys any special tasks and used no programmed stimulation which would have limited the discovery of the unexpected. Our method of testing made it possible to discover the underlying complexity of stimulus-response relationships which cannot be revealed under restricted experimental conditions. However, with our method a detailed analysis of causal relationships was not possible. This could have been done only under such temporally and otherwise controlled experimental conditions that have been used by other investigators (Mountcastle et al., 1975; Lynch et al., 1977; Yin and Mountcastle, 1977; Robinson et al., 1978). Our results may, however, serve further, more quantitative research.

Explanation of the Results by Afferent Connections of Area 7 Response to Somesthetic Stimuli Afferents from area SI terminate in the most rostral part (Jones and Powell, 1970; Vogt and Pandya, 1978) and afferents from SII in the lateral part of area 7 (Pandya and Kuypers, 1969). Many cells in our study had large cutaneous receptive fields. This can be explained by the afferentation from SII where cells have large and bilateral receptive fields (Whitsel et al., 1969). Area 5 sends fibers to medial and lateral parts of area 7 (Pandya and Kuypers, 1969; Jones and Powell, 1970). Sakata et al. (1973) have described cells in area 5 which responded to complex (directional) stimulation of the skin and joints. Similar findings in this work suggest direct interaction between areas 5 and 7b. Of the cells 20 % were classified as responsive to palpation of muscles or stretching of tendons. Since the stimulation could not be restricted to muscles, this result remains rather suggestive. Afferentation from muscles might, however, reach area 7 via SI where cellular responses or evoked potentials have been recorded on stimulation of muscle spindles (Phillips et al., 1971; Burchfiel and Duffy, 1972; Schwarz et al., 1973). The information may pass further through area 5 where cells are responsive to palpation or stretching of muscles (Duffy and Burchfiel, 1971; Sakata et al., 1973; Mountcastle et al., 1975). The projections from the motor and premotor area to area 7b (Pandya and Kuypers, 1969) may also carry somatic information from muscles. Cells responding only to stimuli moving in a certain direction were common in our study. This type of neuron has been recorded also in cortical regions that send somesthetic information to area 7 (SI: Mountcastle et al., 1969; Whitsel et al., 1972; Hyv/irinen and Poranen, in press, SII: Whitsel et al., 1969, area 5: Sakata et al., 1973; Mountcastle et al., 1975).

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Responses to Visual Stimuli Many visual areas send projections to area 7, e.g., areas 18 and 19 in the occipital lobe, areas 20 and 21 in the temporal lobe (Kuypers et al., 1965; Pandya and Kuypers, 1969; Wagor et al., 1975), and the pulvinar (Chow, 1950; Trojanowski and Jacobson, 1976; Divac et al., 1977). Most visually drivable cells in our study responded to moving stimuli in the central visual field and a few cells responded only to moving stimuli in the periphery of the visual field. These two types of cells may have different sources of information in the visual system.

Modulation of Cellular Activity by the "Internal State" of the Monkey Modulation of cellular activity by the level of arousal, motivational or emotional state, or focus of attention could depend on several afferent connections: from the prefrontal cortex, from limbic brainstem pathways (Kievit and Kuypers, 1975; Mesulam et al., 1977), from several nuclei of the thalamus and basal forebrain (Divac et al., 1977; Mesulam et al., 1977), from the cingulate (areas 23, 24) and parahippocampal gyri (area 27) (Jones and Powell, 1970; Nauta, 1971; Mesulam et al., 1977). As has been pointed out by many researchers, a lesion]n the prefrontal cortex causes difficulties in programming actions aimed at a certain goal. One third of our cells discharged only during active movements. They might be under direct influence of the frontal association cortex. These cells might, however, receive afferents also from the premotor and motor cortex ("corollary discharge"). "Laterality" of the Cells Areas 7 have numerous interhemispheric connections (Pandya and Kuypers, 1969; Pandya et al., 1971; Kaas et al., 1977). Ipsilateral afferentation may come also through intrahemispheric connections from SII or area 5. These findings are in accordance with the result that 35 % of our cells were "bilateral".

Restrictions of our Method of Examination Our method of examination had some restrictions which should be taken into consideration when the results are interpreted: 1. We noticed regularly that a group of stimuli which were similar in spatio-temporal appearance or other information content could activate the same cell in varying degrees. Quantitative estimation of the differences was not, however, possible because of the nonstandardized stimuli. Since we did not use the histogram technique, only clear and strong responses could be observed and analyzed. 2. The vestibular system was not studied. The properties of all the cells were examined when the monkey was sitting upright. Therefore, it could not be concluded whether it was the visual or vestibular (or neither of them) that constituted the frame of

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reference for a cell which responded, for instance, both to cutaneous and visual stimuli moving downwards in the gravity field. 3. We could not determine the exact temporal relationships between the stimuli and cellular responses or between cellular activity and the corresponding motor behavior (except for eye movements). This rendered the evaluation of causal relationships of the following phenomenon difficult. Of the cells 30 % were active only during the monkey's own movements, and the cellular activity was apparently independent of the exact execution of the movement although it was dependent on the movement of a certain part of the body. We suggest that their activity is an antecedent of the action. Our experimental conditions did not, however, warrant the exclusion of three alternative explanations: (a) these cells responded to sensory stimuli which we could not produce by passive stimulation, (b) these cells responded to sensory feed-back during active movements (gating phenomenon), (c) they monitored activity of the premotor or motor cortex (corollary discharge). Mountcastle et al. (1975) and Lynch et al. (1977) have documented well the temporal relationships between the cellular activity, eye movements, and visual stimuli and showed that the cellular activity related to eye movements started before the movement. They interpreted that these neurons have a "command function", e.g., they are a cause of the action. 4. The dependence of cellular activity on repetition of stimulation or internal state of the monkey was not systematically studied. However, our observations and the experiments conducted on a few cells made it evident that these factors influence cellular activity in area 7.

Results in the Light of Ablation Studies It is known from ablation studies in man that lesions in different parts of the parietal association cortex result in different symptoms. This suggests that there is functional differentiation within this area. Is there functional differentiation within area 7 in the monkey? We suggest that the discrepancy between findings in anatomically different areas (e.g., our findings versus those of Lynch et al.) is an indication of a functional differentiation within area 7. The medial part of area 7 seems to be specialized in the control of eye movements whereas the lateral part is specialized in the control of arm movements. It is known from ablation studies that the parietal association cortex participates in spatial analysis and spatial control of movements. How does the activity of single cells reflect this function? We found that most cells responded to stimuli moving in a certain direction which, as we suggest, indicates that area 7b carries out spatial analysis. We also found that some cells received information through several sensory channels and that the directions of stimuli moving across the receptive field of one sensory system were analyzed in reference to the coordinates of another system. This made it possible for a "convergence" cell (under restricted conditions) to respond selectively to stimuli whose directions of movement were the same (parallel) in the objective world even when the stimuli were presented to different sensory systems (exteroceptive, proprioceptive, visual). Furthermore, it was found that the

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activity of most cells was related to receptive or motor functions of the arms. Thus, we suggest that area 7b is specialized in spatial control of arm m o v e m e n t s .

Acknowledgements. This work has been supported by a grant from the Academy of Finland, Research Council for Medical Sciences. We thank Mrs. Katriina Lauren and Mrs. Ritva Kettunen for helpful technical assistance.

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