EXPERIMENTAL

NEUROLOGY

48, 57-78 (1975)

Population Analysis of Single Units in the Cuneate Nucleus of the Cat P.

BLUM,

M. B.

BROMBERG

Department of Physiology University of Vermont,

AND

and Biophysics, Burlington:,

Received January

D.

WHITEHORN

College Vermont

1

of Medicine, 05401

31, 1975

Population analysis has been used to investigate the properties of cells in the cuneate nucleus of the chloralose-anesthetized cat. Postsynaptic units were grouped on the basis of the maximum frequency following to ipsilateral superficial radial nerve stimulation, the degree of convergence onto cells from central and peripheral sources, and the response to natural stimulation of the ipsilateral forelimb. The groups were analyzed further on the basis of depth in the brainstem, initial spike latency, and variability in the initial spike latency in response to stimulation of the ipsilateral forelimb. Maximum order to the data resulted when the cells were grouped on the basis of maximum frequency following ability. The possible role of the defined cell groups in production of primary afferent depolarization (PAD) was examined by constructing simulated PAD time course curves. Both a rapidly rising time course curve, typical of ipsilateral forelimb activation, and a slowly rising curve, typical of “off-focus” activation, could be obtained by linearly summing unit depolarizations in a temporal pattern defined by measured spike latencies to the appropriate input. This, and other evidence, suggest that the observed properties of cuneate inhibition can be accounted for by the activity of cells within the cuneate nucleus. A wiring diagram for cuneate inhibition circuitry is presented.

INTRODUCTION The functional cell types of the dorsal column nuclei and their interconnections have been under study for a number of years. Most models 1 This paper is based on part of a dissertation by the first author in partial fulfillment of the requirements for the Ph.D. degree. The work was supported by a USPHS grant NS 09472 and NS 05082 from the National Institute for Neurological Diseases and Stroke. We thank James Walsh for his assistance in the early experiments, Peter McCarthy for the photography, and Louise Alhadeff for typing the manuscript. The present address of Dr. Blum is: Department of Neurology, College of Physicians and Surgeons, Columbia University, 630 West 168th Street, New York, New York 10032. The present address of Dr. Bromberg is: Department of Physiology and Biophysics, School of Medicine, University of Washington, Seattle, Washington 98195.

Copyright All rights

1975 by Academic Press, Inc. o3 reproduction in any form reserved.

58

BLUM,

BROMBERG

AND

WHITEHORN

include two cell types: relay cells, which transmit information from the periphery to the thalamus; and interneurons, which serve to inhibit relay cells by presynaptic and postsynaptic mechanisms (2). An alternative to this arrangement was made by Towe (27). This report presents a population analysis of cuneate neurons recorded in the region of the obex. It has been found previously that neurons in this region include both relay cells and interneurons (11) ; they receive peripheral input from primary and secondary afferent fibers (19), and they have central input from both cerebral cortex and reticular formation (17,22). In this study, cells were characterized by their response properties to natural and electrical stimulation of the periphery and electrical stimulation of central structures. When the properties of the cells were considered, two distinct subsets could be defined: one was characterized by high frequency following ability, short initial spike latency and little convergence; the other by poor frequency following, longer latency and convergence from widespread areas of the body surface and from many central structures. Studies of the time course of inhibition in the dorsal column nuclei suggest the presence of two subpopulations of neurons. Presynaptic and postsynaptic inhibition evoked from the ipsilateral (on focus) periphery rises to peak faster than that evoked from the cortex (1)) reticular formation (9), off-focus periphery (16) and other regions (13, 24). In a quantitative study of the time course of primary afferent depolarization (PAD) in the cuneate nucleus, no difference was found in the time to maximum depolarization evoked by stimulation of the cortex or contralateral forepaw. The time to maximum depolarization evoked by stimulation of the ipsilateral periphery, however, occurred significantly earlier (7). Further, it has been suggested that a portion of the reticular formation is involved in mediating inhibition from widespread sources, either by sending inhibitory axons to the dorsal column nuclei (16) or by serving to excite inhibitory neurons within the dorsal column nuclei (10). It is proposed that the subsets defined here are responsible for mediating the two different inhibitory effects described. The data are consistent with the postulate that cells mediating inhibition are located within the cuneate nucleus. Preliminary reports of this work have been published (4, 5). METHODS Adult cats were anesthetized with alpha-chloralose (60 mg/kg, ip) , paralyzed with Flaxedil and artificially ventilated. Body temperature was maintained between 36 and 38 C. Sti~nulation. The ipsilateral superficial radial nerve was stimulated above

CUNEATE

NEURONS

59

the wrist with bipolar silver hook electrodes for cell detection and subsequent testing (0.05-msec square pulses, l-10 ma). The central paw pad of from one to three of the other (off-focus) limbs was activated by bipolar needle electrodes (l-cm separation, 1-msecpulses, l-10 ma). In the medial Iemniscus, either bipolar electrodes (OS-mm exposed lead. 0.5mm tip separation), or bipolar concentric electrodes (shaft diameter 0.5 mm, center diameter 0.2 mm) with resistancesbetween 30 and 50 Kfl were placed stereotaxically (A = 4.0, M = 6.0, H about -1) to test for cuneothalamic projection. An electrode was judged to be property positioned in the medial lemniscus when an intially negative wave with short latency (4 msec) was recorded which followed 100-Hz stimulation of the ipsilateral superficial radial nerve and from which a crisp, multiunit discharge was evoked after tactile stimulation of the ipsilateral forelimb. The position was verified histologically. The inferior cerebellar peduncle was stimulated with a bipolar electrode placed at coordinates A = 0, M = 6.5, H = 3.5 (23). A series of predetermined natural stimuli were applied to the skin and hair of the ipsilateral forepaw or contralateral forepaw (or both) for each unit in order to detect the influences of receptor types that are known to ascend to the level of the brainstem directly from the periphery (S, 20). Single Unit Recording. The dorsal surface of the cuneate nucleus was exposed, and a caudal piece of the cerebellum was ablated by suction until the rostra1 portion of the cuneate nucleus was visible. Single unit extracellular recordings were made with glass microelectrodes (2 to 10 mn) filled with either 4 M NaCl or a saturated solution of fast green dye in 2 M NaCl. The recording electrode was moved in the rostrocaudal direction in 0.5 mm steps with the obex as the point of reference. Pulsations of the brainstem were reduced by a pneumothorax and by pouring justmolten paraffin wax (m.p.

Population analysis of single units in the cuneate nucleus of the cat.

EXPERIMENTAL NEUROLOGY 48, 57-78 (1975) Population Analysis of Single Units in the Cuneate Nucleus of the Cat P. BLUM, M. B. BROMBERG Departmen...
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