Interaction of direct afferent and recurrent signals in cat motor cortex neurons

Intracellular activity was recorded from the functionally identified motor cortex neurons (MI, area 4) in acute experiments on myorelaxin-immobilized cats under calypsol anesthesia. Changes in neuronal responses to testing stimulation of the ventrolateral thalamic nucleus or pyramidal tract fibers were studied; the same or another input was used for a conditioning stimulation. Excitatory and inhibitory components of test responses of variousMI neurons were found to be either facilitated or depressed. The facilitation of orthodromic excitation was more frequent in the case of thalamic testing stimulation. The depression of both excitatory and inhibitory components of the response was more pronounced with paired stimulation of the pyramidal tract fibers. The peculiarities of interaction between direct afferent and recurrent signals in theMI neurons are thought to be determined by different distribution of thalamocortical fiber terminals and recurrent collaterals of corticofugal axons in the cortex and nonuniform localization of their synapses on dendrites and somata of the studied cells. It seems possible that these peculiarities also are connected with different chemical mechanisms of synaptic transmission in the above synapses and different properties of postsynaptic membrane receptors.Neirofiziologiya/Neurophysiology, Vol. 26, No. 3, pp. 203–210, May–June, 1994.     

Studies of directional sensitivity of neurons in the cat primary auditory cortex

A set of impulsive transient signals has been synthesized for earphone delivery whose waveform and amplitude spectra, measured at the eardrum, mimic those of sounds arriving from a free-field source. The complete stimulus set forms a "virtual acoustic space" (VAS) for the cat. VAS stimuli are delivered via calibrated earphones sealed into the external meatus in cats under barbiturate anesthesia. Neurons recorded extracellularly in primary (AI) auditory cortex exhibit sensitivity to the direction of sound in VAS. The aggregation of effective sound directions forms a virtual space receptive field (VSRF). At about 20 dB above minimal threshold, VSRFs recorded in otherwise quiet and anechoic space fall into categories based on spatial dimension and location. The size, shape and location of VSRFs remain stable over many hours of recording and are found to be shaped by excitatory and inhibitory interactions of activity arriving from the two ears. Within the VSRF response latency and strength vary systematically with stimulus direction. In an ensemble of such neurons these functional gradients provide information about stimulus direction, which closely accounts for a human listener's spatial acuity. Raising stimulus intensity, introducing continuous background noise or presenting a conditioning stimulus all influence the extent of the VSRF but leave intact the gradient structure of the field. These and other findings suggest that such functional gradients in VSRFs of ensembles of AI neurons are instrumental in coding sound direction and robust enough to overcome interference from competing environmental sounds.     

Mapping the effects of SI cortex stimulation on somatosensory relay neurons in the rat thalamus: direct responses and afferent modulation

We have used single-unit recording techniques to map the spatial distribution of the primary somatosensory (SI) cortical influences on thalamic somatosensory relay nuclei in the rat. A total of 193 microelectrode penetrations were made to record single neurons in tracks through the medial and lateral ventroposterior (VPL and VPM), ventrolateral (VL), posterior (Po), and reticular (nRt) thalamic nuclei. Single units were classified according to their (1) location within the nuclei, (2) receptive fields, and (3) response to standardized microstimulation in deep layers of the SI cortical forepaw areas. The SI stimulation produced short-latency (1- to 7-msec) excitatory responses in different percentages of neurons recorded in the following thalamic nuclei: VPL, 42.0%; Po, 25.0%; nRt, 16.4%; VL, 13.6%; and VPM, 9.9%. Within the VPL, the highest proportion of responsive neurons was found in the anterior region. Although most of the VL region was unresponsive, the caudal subregion bordering the rostral VPL showed some responsiveness (13.6% of neurons). In general, the spatial pattern of corticothalamic influences appeared to reciprocate the known thalamocortical connection patterns, but with a heterogeneity that was unpredicted. The same parameters of SI cortical stimulation were used in studies of corticofugal modulation of afferent transmission through the VPL thalamus. A condition-test (C-T) paradigm was implemented in which the cortical stimulation (C) was delivered at a range of time intervals before test (T) mechanical vibratory stimulation was applied to digit 4 of the contralateral forepaw. The time course of cortical effects was analyzed by measuring the averaged evoked unit responses of thalamic neurons to the T stimuli, and plotting them as a function of C-T intervals from 5 to 50 msec. Of the 20 VPL neurons tested during SI stimulation, the average response to T stimulation was decreased a mean of 36%, with the suppression peaking (at 49% inhibition of the afferent response) about 15 msec after the C stimulus. Considerable rostrocaudal variation was observed, however. Whereas neurons in the rostral VPL (near VL) were strongly inhibited (-69%), neurons in the middle and caudal VPL exhibited facilitations at long and short C-T intervals, respectively. This study establishes a specific projection system from the forepaw region of SI cortex to different subregions of the VPL thalamus, producing specific temporal patterns of sensory modulation.     

Responses of neurons in cat primary somatosensory cortex to repetitive stimulation of vibrissae

Extra- and intracellular responses of neurons in the primary somatosensory cortex to repetitive mechanical stimulation of the vibrissae at different frequencies were studied in unanesthetized curarized adult cats. Unlike responses to electrical stimulation of the combined afferent input (the infraorbital nerve) spike discharges of neurons in response to vibrissal stimulation can reproduce rather higher frequencies of stimulation and their initial character changes more often in the course of the repetitive series. Most cortical neurons were characterized by limitation of the area of their peripheral receptive fields with an increase in the frequency of adequate repetitive stimulation. A group of cortical neurons was distinguished by its ability to respond to high-frequency stimulation and to generate burst discharges. Comparison of the frequency characteristics of spike responses of these cells and of inhibitory synaptic action in other cortical neurons led to the conclusion that this group of cells thus distinguished may be inhibitory cortical neurons. The role of interaction between excitatory and inhibitory processes arising in cortical neurons during repetitive stimulation of different areas of their receptive fields is discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 14, No. 2, pp. 164–171, March–April, 1982.     

Characteristics of poststimulus and lateral inhibition in neurons of cat primary auditory cortex

Experiments using intracellular recording of potentials from neurons of the primary auditory cortex of cats anesthetized with pentobarbital showed that under the influence of tones of characteristic frequency for the neuron under test, or of electrical stimulation of nerve fibers of the spiral ganglion, innervating the center of the receptive field of the neuron, transient excitation of the latter is followed by the development of prolonged (20–250 msec) inhibition. The cause of this inhibition is an IPSP arising in the neuron after the action potential. On the basis of data showing a close connection between inhibition and the preceding spike it is concluded that it arises through the participation of a mechanism of recurrent inhibition. During the action of tones of uncharacteristic frequency or electrical stimulation of the peripheral part of the receptive field of the neuron, a response consisting of EPSP-IPSP arises in the neuron. This IPSP is accompanied by inhibition of spontaneous activity of the neuron and its responses to testing stimulation. It has been shown that this inhibition is lateral in its genesis. Characteristics of these two types of inhibition are given.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 16, No. 2, pp. 194–201, March–April, 1984.     

Horseradish peroxidase-positive neurons of nonspecific thalamic nuclei projecting to the primary somatosensory cortex in cats

The morphology and topography of neurons whose axons form the nonspecific thalamic input in the primary somatosensory area were studied in the cat forebrain by the retrograde axonal horseradish peroxidase transport method. Stained cells were found in the dorsolateral part of the nucleus ventralis anterior, and were diffusely distributed in the nucleus centralis, lateralis, the lateral part of the nucleus dorsalis medialis, and the dorsal part of the centrum medianum. In the nucleus paracentralis only solitary, palely stained neurons were detected. Cells stained with horse-radish peroxidase were multipolar, triangular, or fusiform. The results are evidence that besides the ventrobasal complex, the nonspecific nuclei of the diencephalon also project into the somatosensory cortex. This indicates the existence of multiple afferent thalamic inputs into the somatic cortex.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 11, No. 5, pp. 435–440, September–October, 1979.     

Morphological characteristics of callosal neurons of the cat primary auditory cortex (AI)

Cortical stratification of neurons forming callosal projections to the primary cortical area (AI) was investigated in cats using horseradish peroxidase axonal transport techniques. The population of area AI callosal neurons was found to be composed of several groups of cells. The group comprising around 60% of all callosal neurons of this area consists of large layer III pyramidal neurons. Callosal neurons belonging to this layer have a mean perikaryon profile area of 261.8±8.2 µm²; they account for 22% of all cells found in the layer. The second group, comprising 27% of all area AI callosal neurons, was largely made up of large layer V and VI cells; these could not be classed as pyramidal neurons due to the shape of their somata and the geometry of their dendritic arborization. Perikaryon profile in these nonpyramidal neurons occupied an area of 250.3±8.4 µ². No callosal neurons were observed in layer I. These account for 6 and 7% of total numbers of callosal neurons of area AI in layers II and IV. Callosal neurons were found to form projections to all layers of area AI in the contralateral hemisphere. Highest density of callosal fiber endings was observed in layers II and III.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 22, No. 2, pp. 249–256, March–April, 1990.     

Interaction between neurons displaying tonic response to sound and other cells of the feline auditory cortex

Interaction between neurons with a tonic response pattern and either nearby or further removed (by about 400–500 µm) cortical neurons was investigated during acute experiments on 15 immobilized cats using cross-correlation analysis techniques. Synchronizing excitatory input common to the nerve cells was found in cross-correlation histograms (CCH) in 26 out of 36 test pairs of neurons (72%). Both positive and negative cross-correlation (five pairs in each case) were discovered, pointing to mono- or polysynaptic excitatory and inhibitory effects of the tonic neuron on spike activity in the other cell from CCH of 10 pairs of neurons. The functional diversity of neurons f distinguished by a tonic pattern of response to sound was deduced on the basis of findings from this research. The theory that some tonic type cells act as excitatory neurons and others fulfil the function of inhibitory interneurons is examined.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 21, No. 5, pp. 613–620, September–October, 1989.     

Responses of neurons in the primary auditory cortex of the cat to the auditory motion stimuli with variable interaural delay

Unit responses in the primary auditory cortex of anesthetized cats to stationary and apparently moving stimuli resulted from a static and dynamically varying interaural delay (ITD) were recorded. The static stimuli consisted of binaurally presented tones and clicks. The dynamic stimuli were produced by in-phase and out-of-phase binaurally presented click trains with time-varying ITD. Sensitivity to ITDs was mostly seen in responses of the neurons with low characteristic frequency (below 2.8 kHz). All cells sampled with static stimuli responded to simulated motion. A motion effect could take the form of a difference in response magnitude depending on the direction of stimulus motion and a shift in the ITD-function opposite the direction of motion. The magnitude of motion effects was influenced by the position of motion trajectory relative to the ITD-function. The greatest motion effect was produced by motion crossing the ITD-function slopes.     

Predicting spike occurrence and neuronal responsiveness from LFPs in primary somatosensory cortex

Local Field Potentials (LFPs) integrate multiple neuronal events like synaptic inputs and intracellular potentials. LFP spatiotemporal features are particularly relevant in view of their applications both in research (e.g. for understanding brain rhythms, inter-areal neural communication and neuronal coding) and in the clinics (e.g. for improving invasive Brain-Machine Interface devices). However the relation between LFPs and spikes is complex and not fully understood. As spikes represent the fundamental currency of neuronal communication this gap in knowledge strongly limits our comprehension of neuronal phenomena underlying LFPs. We investigated the LFP-spike relation during tactile stimulation in primary somatosensory (S-I) cortex in the rat. First we quantified how reliably LFPs and spikes code for a stimulus occurrence. Then we used the information obtained from our analyses to design a predictive model for spike occurrence based on LFP inputs. The model was endowed with a flexible meta-structure whose exact form, both in parameters and structure, was estimated by using a multi-objective optimization strategy. Our method provided a set of nonlinear simple equations that maximized the match between models and true neurons in terms of spike timings and Peri Stimulus Time Histograms. We found that both LFPs and spikes can code for stimulus occurrence with millisecond precision, showing, however, high variability. Spike patterns were predicted significantly above chance for 75% of the neurons analysed. Crucially, the level of prediction accuracy depended on the reliability in coding for the stimulus occurrence. The best predictions were obtained when both spikes and LFPs were highly responsive to the stimuli. Spike reliability is known to depend on neuron intrinsic properties (i.e. on channel noise) and on spontaneous local network fluctuations. Our results suggest that the latter, measured through the LFP response variability, play a dominant role.     

Bilateral receptive field neurons and callosal connections in the somatosensory cortex

Earlier studies recording single neuronal activity with bilateral receptive fields in the primary somatosensory cortex of monkeys and cats agreed that the bilateral receptive fields were related exclusively to the body midline and that the ipsilateral information reaches the cortex via callosal connections since they are dense in the cortical region representing the midline structures of the body while practically absent in the regions representing the distal extremities. We recently found a substantial number of neurons with bilateral receptive fields on hand digits, shoulders-arms or legs-feet in the caudalmost part (areas 2 and 5) of the postcentral gyrus in awake Japanese monkeys (Macaca fuscata). I review these results, discuss the functional implications of this bilateral representation in the postcentral somatosensory cortex from a behavioural standpoint and give a new interpretation to the midline fusion theory.     

Ultrastructural characteristics of layer III pyramidal neurons in the cat primary auditory cortex (Al)

Electron microscope studies were made of retrogradely horseradish peroxidase-labeled pyramidal neurons forming transcallosal projections in layer III of the cat primary auditory cortex (Al). These showed a significant proportion of the somatic membrane to be covered with processes of astroglia, while synapses occupy 20% of the synaptic surface on average. Between 4 and 10 axosomatic synapses were identified on the profiles of callosal cell somata. All these were formed by axonal terminals containing small, flattened synaptic vesicles and had symmetrical contacts. Average length of these synaptic contacts equaled 1.6 µm. Numerous anterogradely horseradish peroxidase-labeled axonal terminals of callosal fibers were found in cortical area Al in amongst retrogradely HP-labeled neurons. The ultrastructural pattern of these is described.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 22, No. 4, pp. 520–526, July–August, 1990.     

Interaction of heterosensory afferent impulses on neurons of thalamic associative nuclei

The character and particular features of interaction between visual, auditory, and electrodermal afferent impulses on neurons of the pulvinar, posterolateral, and mediodorsal thalamic nuclei were studied in acute experiments on cats anesthetized with a mixture of pentobarbital and chloralose. Interaction discovered on cells of both groups of structures was of two types. In the first (the one most frequently found) only inhibition was observed or inhibition followed by facilitation of the response to testing stimulation; in the second type only facilitation or facilitation followed by inhibition of unit activity was found. Overall ability for interaction to take place on neurons of the mediodorsal nucleus was weaker than on cells of the pulvinar-posterolateral complex (P<0.05). Interaction was strongest on trisensory cells; it was also observed on monosensory cells or on cells which did not respond to isolated stimulation.Donetsk Medical Institute. Kemerovo Medical Institute. Translated from Neirofiziologiya, Vol. 10, No. 5, pp. 478–485, September–October, 1978.     

Mastication-related neurons in the orofacial first somatosensory cortex of awake cats

In the orofacial area of the first somatosensory cortex (SI), we recorded single unit activity from 699 neurons in 11 awake cats. Fifty-two percent (362/699) were mastication-related neurons (MRNs) showing activity related to some aspects of masticatory movements. MRNs were divided into three types by their activity patterns: (1) the rhythmical type, showing rhythmical bursts in pace with the masticatory rhythm; (2) the sustained type, showing a sustained firing during the period of taking food and (3) the transient (biting) type, showing intense discharges in coincidence with biting hard food. MRNs had mechanoreceptive fields in the perioral, tongue, periodontal and mandibular regions. The activities of perioral rhythmical-MRNs, mandibular transient-MRNs, tongue rhythmical-MRNs and periodontal transient-MRNs were correlated with food texture, while perioral rhythmical-MRNs, perioral sustained-MRNs and tongue sustained-MRMs were not. Both facial and intraoral MRNs were scattered throughout the facial and intraoral projection areas in SI. These findings provide evidence that the orofacial SI monitors masticatory movements for food ingestion.