A.L. Towe

Extracellular microelectrode sampling bias.

Abstract The antidromic response latencies of 640 pyramidal tract neurons, isolated in pericruciate cortex of the cat, were measured after stimulation of the medullary pyramids. The expected time distribution of antidromic response latencies was then calculated from published values for axon diameters in silver-stained preparations; compensation for shrinkage was not attempted. With conduction velocity assumed to be a linear function of fiber diameter, the optimum fit between the observed and expected antidromic latency distribution was calculated. The constant of proportionality had a value of 4.72, and raising each diameter value to the 2.52 power was found necessary for an optimum fit. Extracellular microelectrode sampling is proposed to be akin to “shooting fish in a barrel,” in the sense that the probability of a successful isolation is largely a function of the cross-sectional area of the axon. Other factors, such as microelectrode resistance and investigator experience and vigilance, play a lesser role. A correction vector, based on the exponent of 2.52 and on histological measurements, was derived for postcruciate tissue, and applied to a sample of 1109 orthodromically activated neurons. This application showed the effect of electrode sampling bias to be significant.

Properties of the pyramidal system in the cat

Abstract Response characteristics of 833 neurons in the pericruciate cortex of the cat were studied to find which sent axons into the medullary pyramids. The traditional criteria for classifying cortical neurons as pyramidal tract neurons were examined and found to be adequate. The population behavior of these neurons was then analyzed. The population was found to segregate into two groups on the basis of both antidromic and orthodromic response properties. A group of early-firing neurons was scattered throughout the cortex, but was concentrated at the level of layer V. A second group of later-firing neurons was found in the upper parts of the cortex, concentrated at the level of layer III. Two distinct afferent inputs appeared to underlie the orthodromic group segregation: Both inputs bombarded the early-firing neurons, but only one of them bombarded the late-firing neurons. A similar grouping of these neurons was observed following stimulation of the ipsilateral forepaw and of both hindpaws. The patterns of activity of these neurons are related to certain properties of the reflex corticofugal discharge recordable from the medullary pyramids.

On the nature of the primary evoked response

The hypothesis that the primary evoked response results from the summation of slow postsynaptic potential changes on synaptically driven neurons near the recording electrode is tested in this research by a computer simulation. On the assumption that cortical resistivity remains relatively constant through depth in the cerebral cortex and through time during afferent input, net current is proportional to gradV. The vertical component of net current flow in the cats somatosensory cortex was measured during the primary evoked response and a method was devised for fractionating this current into a major part, due to s neurons (see footnote 2), and a minor part, due to m neurons. A model of the distribution of extracellular current flow was developed and, with the use of histological and neuronal population response data, the vertical component of net current flow due to s neurons was calculated. The experimentally derived and the calculated patterns of vertical current flow were found to be alike in all major features, thus strongly supporting the hypothesis under test. The weak currents due to m neuron response were not simulated in this study.

Response properties of neurons in the pericruciate cortex of the cat following electrical stimulation of the appendages

Abstract In chloralose-anesthetized cats activity was recorded extracellularly from single neurons isolated in two circumscribed regions of the anterior cerebral hemisphere, one just rostral and the other just caudal to the lateral tip of the cruciate sulcus. Each neuron was classed as either PT or non-PT, depending upon whether or not its axon coursed through the medullary pyramids. The discharge patterns of each neuron were measured following electrical stimulation of the central footpad of each appendage. If the neuron responded to contralateral forepaw stimulation but failed to respond to stimulation of any other appendage, it was classed as an s neuron; if it responded to stimulation of the contralateral forepaw and at least one other appendage, it was classed as an m neuron. PT, s neurons constituted a negligible fraction of the total sample. Both the depth within the cortex and the temporal pattern of discharge of non-PT, s neurons differed markedly from that of m neurons. PT, m and non-PT, m neurons were identical in behavior and are believed to have similar functional significance. The population response of m neurons to stimulation of the ipsilateral forepaw was the same as that following stimulation of the contralateral forepaw—merely delayed a few milliseconds. It is thus concluded that the non-PT, s neurons, which discharge before m neurons, do not drive the m neurons. The s neurons, which do not follow as high input frequencies as do m neurons, are thought to be a functionally distinct population of neurons which inhabits the external granular layers of the cortex. Their activity is closely associated with the surface positive phase of the concomitant primary evoked response. It is suggested on the basis of these experiments that the cortical input is directly linked to the cortical output.

Differential activity among wide-field neurons of the cat postcruciate cerebral cortex

Extracullular recordings were made of the evoked activity of neurons in sensorimotor cortex of cat following cutaneous stimulation of each limb. Neurons responding only to stimulation of the somatotopically “on focus” limb (CFP) were classed as s and separated from those responding to stimulation of at least one additional limb; the latter “wide-field” neurons were classed as m. The ratio of m to s increased from “sensory” to “motor” recording sites. Analysis was focused on m neurons of the postcruciate recording site—here 80% of the pyramidal tract (PT) cells were m neurons. Both “fast” and “slow” PT cells were identified, the latter residing more superficially and firing later than the former. Despite the wide receptive fields of these cells, a unique pattern of PT activity develops in the cortex that is somatotopically related to the cutaneous site of stimulation. This pattern results from a facilitatory action of s neurons on the PT,m elements, particularly the “slow” PT cells. The PT response patterns following stimulation at any other site are remarkably similar and suggest a “coadunating” function either in thalamus or cortex itself. The non-PT,m elements behave in a similar manner. These results restore a measure of somatotopic organization to the wide-field neurons. However, consideration of the anatomical distribution of PT elements and the physiological data supports the hypothesis that the pyramidal-tract elements originating in the postcruciate cortex of the cat serve primarily in an excitability-modulating capacity.

POPULATION AND MODALITY CHARACTERISTICS OF NEURONS IN THE CORONAL REGION OF SOMATOSENSORY AREA I OF THE CAT.

By extracellular microelectrode techniques, neurons were isolated within the forepaw receiving area of primary somatosensory area I of the cat, just medial to the caudal end of the coronal sulcus. The response properties of 278 neurons were studied from several aspects, including: (a) modality specificity; (b) location and extent of receptive field; (c) responsiveness to direct electrical stimulation of the skin; (d) ability to follow iterative electrical stimulation; and (e) locus of isolation within the cortical tissue. Eighty-two per cent of the neurons responded to touch but not hair stimulation; only 6% were classed as hair sensitive. The receptive fields were uniformly small, the largest identified being 8 cm2, and were located mainly on the distal parts of the forelimb. All these neurons responded to electrical stimulation of the skin, and all tested responded to direct electrical stimulation of the cuneate nucleus. A population analysis revealed that the greatest amount of neuron activity following stimulation of the contralateral forepaw occurred 0.6–0.9 mm below the pial surface, 11–13 msec after the stimulus. The population pattern of response to direct stimulation of the cuneate nucleus was identical to that following contralateral forepaw stimulation—merely shifted 5.2 msec earlier in time. The positive phase of the surface recorded primary evoked response occurred during this peak activity. It is concluded that the afferent input to this region of the cortex comes entirely by way of the dorsal column-medial lemniscus system, for no other afferent influence was found necessary to explain the response pattern. The population response pattern is compared with that from the postcruciate cortex and found to be strikingly different. However, the coronal neuron population displayed an affinity to one particular subset of neurons isolated in more rostral and medial cortex.

Control of Somatosensory Input by Cerebral Cortex

Direct stimulation of the pyramidal tract increases the size of the excitatory receptive fields of neurons in the somatosensory cortex of the cat. This effect reflects greater transmission of cutaneous information through the dorsal column nuclei as a result of the facilitation of cells in these nuclei by pyramidal tract fibers.

Wide-field neurons in thalamic nucleus ventralis posterolateralis of the cat.

Abstract Gross evoked potentials and the concomitant single neuron responses were recorded from the anterior half of nucleus ventralis posterolateralis (VPL) of the thalamus in chloralose-anesthetized cats. Responses were evoked by stimulation of the skin on either side of the body and by stimulation of the ipsilateral and contralateral dorsal funiculi. The latency and configuration of the gross evoked potentials differed according to the limb stimulated, but the same pattern of configurations, at shorter latencies, could be produced by weak stimulation of the four dorsal spinal fasciculi. Furthermore, with only one exception, each neuron was found to be specifically responsive to stimulation of the dorsal spinal fasciculus (or fasciculi) that carried afferent fibers from its cutaneous excitatory receptive field. Anatomical, histological, and functional criteria showed that the sample was drawn from within nucleus VPL. Two-thirds of the sample comprised small-field neurons, and fully 30% of the sample comprised neurons with bilateral excitatory receptive fields. The correlations of response latency to cutaneous and dorsal funicular stimulation were high for all types of neurons. Routine stimulation of the opposite nucleus VPL revealed that only neurons with an ipsilateral component to their excitatory receptive fields were excitable via that route. Occasional test shocks to the dorsolateral funiculi revealed that many wide-field, but few small-field, neurons could be excited via that route. After discussing the implications of these findings, it is concluded that the dorsal funicular-medial lemniscal system comprises the main substrate for both the contralateral and ipsilateral responsiveness of nucleus VPL, as seen in the chloralose-anesthetized cat.

Postsynaptic potential patterns evoked upon cells in sensorimotor cortex of cat by stimulation at the periphery

Intracellular and extracellular recordings were obtained from neurons in the sensorimotor forepaw cortex of chloralose-anesthetized, domestic cats. Cells responding with either spike or slow potential activity only after stimulation of the contralateral forepaw were classified as s neurons; those responding additionally after stimulation of other extremities were classed as m neurons. The postsynaptic potential changes evoked by single electric shock to the central footpad of each limb were of particular interest. Seven of the eight well-isolated s neurons responded to contralateral forepaw shock with a long duration depolarization; one responded with a short duration EPSP, followed immediately by a Cl−-dependent hyperpolarization. No intracellular membrane potential changes were seen on the s neurons after stimulation of other limbs. The typical response of m neurons to stimulation of any limb was a long-duration EPSP, followed by a long, weak IPSP. The IPSP was most prominent after contralateral forepaw shock, occasionally being indistinct after stimulation of other limbs. Although the inhibition typically follows an EPSP, 5 of 83 neurons responded to contralateral forepaw shock with an initial hyperpolarization. The observations are used to evaluate four possible mechanisms for the production of cortical inhibition. The data are best interpreted as resulting from a direct, thalamocortical inhibitory projection; the data are inconsistent with an intracortical, “recurrent” model.

Observations on single neurons recorded in the sigmoid gyri of awake, nonparalyzed cats.

Abstract Extracellular recordings were made from 230 single neurons isolated in three regions of the sensorimotor cerebral cortex of awake, unparalyzed cats. The microdrive receptacle was affixed to the skull of each cat during aspetic surgery, and the recordings were done with the cat held in a net hammock. Cats rapidly adapted to the recording situation, often dozing or falling asleep during the recording session. Neuronal activity was evoked by forelimb manipulation. Once isolated, the size and configuration of the excitatory receptive field was determined, using various forms of natural stimulation; any spontaneous activity was also recorded. The neurons responded to discrete stimulation with a burst of spikes; a few showed sustained discharge to prolonged cutaneous stimulation. The excitatory receptive fields were continuous and were either confined to the contralateral forelimb, occupied both forelimbs and the thorax, or included the whole body surface. The behavior of some additional neurons during intravenous anesthetic injection, during electrical stimulation of limb nerves via surgically implanted electrodes, and during sleep-wake cycles was also examined. The similarities and differences between samples from anesthetized and from awake, unparalyzed cats are discussed.