Hierarchical somesthetic processing of tongue inputs in the postcentral somatosensory cortex of conscious macaque monkeys

The representation of the oral structures in the lateralmost part of the postcentral somatosensory cortex in conscious macaque monkeys was studied by recording the activities of single neurons. A total of 104 penetrations were made in the oral regions of six hemispheres in four animals and 2,292 neurons were isolated. The characteristics of the receptive fields (RF) of 1,598 neurons were identified. Of them, 513 neurons (area 3b, 196; area 1, 104; area 2, 213) along 44 penetrations responded to mechanical stimulation of the tongue (tongue neurons). The relative incidence of tongue neurons that had bilateral RFs increased gradually (bilateral integration) on moving caudally from area 3b to area 2. There was also a tendency for the RFs on the tongue to expand in the anteroposterior axis of the tongue (anteroposterior integration). Furthermore, the relative incidence of tongue neurons with composite RFs covering both the tongue and other surrounding oral structures was significantly higher in area 2 than in areas 3b and 1 (interstructural integration). As a result of the bilateral, anteroposterior and interstructural integration, the extent of the RFs of tongue neurons increased progressively from area 3b to area 2. We therefore concluded that hierarchical somatosensory processing, which has been established in the postcentral somatosensory cortex representing other body parts, is also present in the oral representation. We speculate that the hierarchical scheme in the oral representation might be a prerequisite neural process for the oral stereognosis that eventually takes place in the association cortices. Electronic Publication     

Representation of the midline trunk, bilateral arms, and shoulders in the monkey postcentral somatosensory cortex

 Single neuronal activities were recorded in the arm/trunk region of the postcentral gyrus in awake Japanese monkeys. A total of 1608 units were isolated from four hemispheres of two animals, and receptive fields (RFs) and submodalities were identified in 1162 units. Deep or skin submodality neurons were dominant in area 3a or area 3b, respectively. The deep/skin ratio increased as the recording site moved from area 3b to the more caudal areas. In areas 3a and 3b, neuronal RFs were almost exclusively on either the arm or trunk. In areas 2 and 5, neurons with RFs on the trunk decreased and those with RFs on the hand or covering more than one body part, etc. increased. We found a total of 107 neurons with bilateral RFs and 56 with ipsilateral RFs, while the rest (n=999) were with contralateral RFs. Bilateral or ipsilateral neurons of skin submodality (n=37) were found in areas 1, 2, and 5. Twenty six (70%) had RFs on the trunk and/or occiput, five on the forelimb, and the rest (n=6) on both the trunk and forelimb (the combined type). Among 33 skin bilateral neurons, 90% (n=30) had RFs across the midline. Bilateral or ipsilateral neurons responding to joint manipulation (n=104) were found in areas 2 and 5. Most of them were activated by manipulation of the shoulder and/or elbow (the proximal type, n=72, 69%). There were 25 neurons of the combined type (both the proximal and distal joints were effective, 24%). Bilateral or ipsilateral neurons of deep-others submodality (n=20) were found in areas 1, 2, and 5. The forelimb type (n=12, 60%) was dominant in this category. The combined-type neurons in both the skin- and joint-manipulation categories were found only or mostly in area 5. These results indicate the presence of hierarchical processing for bilateral as well as contralateral information within the arm/trunk region of the postcentral gyrus. Received: 12 January 1998 / Accepted: 19 May 1998     

Rostrocaudal gradients in the neuronal receptive field complexity in the finger region of the alert monkey's postcentral gyrus

Summary In the primate postcentral gyrus, the cytoarchitectonic characteristics gradually shift from those of koniocortex to more homotypical parakoniocortex along its rostrocaudal axis. To find the physiological correlates of these changes we examined a large body of data accumulated during a series of our experiments with alert monkeys. Along the rostrocaudal axis of the postcentral gyrus, we found a gradual and continuous increase in the number of neurons with converging receptive fields and those in which receptive field positions or submodalities were not determined. Deep or skin submodality neurons were dominant in area 3a or 3b respectively. The proportion of skin submodality neurons decreased gradually from area 3b to the more caudal part of the gyrus. The proportion of deep submodality neurons was almost constant from area 3b to area 2 inclusive; they were not the majority in area 2. The data are consistent with the hierarchical scheme, i.e., within the postcentral gyrus sensory information is processed from the primary sensory receiving stage to the more associative, integrative stages.     

Bilateral receptive fields of cells in rat Sm1 cortex

Summary Single cells in the primary somatosensory (Sm1) cortex were investigated for responses to bilateral hindpaw stimulation in Wistar rats anaesthetised by continuous intravenous administration of Althesin. Fifty-one percent of cells sampled (N = 134) responded to equivalent punctate mechanical stimuli delivered to both the contralateral and ipsilateral hindpaws under light anaesthesia. The distribution by cortical depth of cells with receptive fields (RFs) on both hindpaws was not significantly different from cells which had only contralateral RFs. No cell was found with a purely ipsilateral RF. For 86% of cells tested (N=44) the ipsilateral RF was partly or completely homologous with areas within the contralateral RF. The sizes of ipsilateral RFs were smaller on 66% of occasions when tested against their contralateral RFs. Modal latencies to ipsilateral mechanical stimulation were longer than to contralateral stimulation (34.1±9.1 ms (S.D) cf. 26.4±7.2 ms, N=44). Ipsilateral RFs were lost for 77% of cells tested following a 33% increase in anaesthetic infusion rate. Conditioning mechanical stimuli applied to the centre receptive field (CRF) on the ipsilateral hindpaw reduced or abolished a cell's responses to equivalent test stimuli applied to it's contralateral CRF with C-T intervals of 20–200 ms. Conditioning stimuli applied to the CRF contralateral to the cell reduced or abolished responses to test stimuli on the cell's ipsilateral CRF using C-T intervals of 0–900 ms. Responses in one cortex to stimulation of the ipsilateral hindpaw were unaffected by elimination of responses from the same hindpaw in the opposite contralateral Sm1 cortex, where responses had been suppressed by topical Lignocaine administration. Retrograde transport of horseradish peroxidase from hindpaw Sm1 cortex labelled many cells in homolateral thalamus, but failed to label cells in the entire forebrain contralateral to the injection site. It is concluded that direct crossed thalamocortical and callosal Sm1-Sm1 pathways do not contribute to the production of hindpaw ipsilateral receptive fields.     

Neuronal responses from beyond the classic receptive field in V1 of alert monkeys

Responses of primary visual cortex (V1) neurons to stimuli inside the classic receptive field (CRF) can be modulated by stimuli outside the CRF. We recently reported that responses of most V1 neurons to a line in the CRF center are inhibited by large surround-stimuli and that this modulation is stimulus selective. Here we report that a significant proportion of V1 neurons in alert monkeys respond directly to stimuli outside the CRF with very long latency and much reduced selectivity. When surround stimuli are presented alone, three response patterns can be distinguished in 153 single- or multiunits tested: (1) 31.4% have no significant response; (2) 50.3% show excitatory responses that are significantly higher than spontaneous activity. The average latency of these responses is about 145 ms, 2–3 times longer than center responses; (3) 18.3% show suppressed spontaneous activity after stimulus onset. The direct surround responses are found to be only weakly selective for the orientation of contextual lines, and not selective for other contextual patterns tested. While the outburst of responses to stimuli within the CRF is not affected by reducing stimulus duration from 500 ms to 50 ms, late excitatory surround responses are virtually eliminated. We propose that the late excitatory surround responses to extra-CRF stimulation alone are the reflection of feedback from higher cortical areas and may contribute to reduced contextual inhibition of cells in V1. This could play a role in figure-ground segregation. Electronic Publication     

Diversity in receptive field properties of vertical neuronal arrays in the crown of the postcentral gyrus of the conscious monkey

Summary Single neuronal activity was recorded in the crown of the postcentral gyrus (areas 1 and 2) in 5 conscious monkeys. A total of 93 penetrations were made in the hand and finger region of 9 hemispheres and 827 neurons were isolated. The receptive field characteristics of neurons recorded along each of 88 penetrations which entered perpendicularly to the cortical surface were compared. The majority of neurons in this region were responsive to skin stimulation. In 54 penetrations, neurons related to different sensory submodalities were mixed. In 30, skin neurons predominated, and in 8, deep neurons, while in the remaining 16 penetrations neurons related to different submodalities were equally mixed. In 16 penetrations, neurons responded exclusively to stimulation of skin, hair or nails. In 9 penetrations, neurons were exclusively related to joint manipulation or other types of deep submodality. In 9 penetrations, unidentified neurons were in the majority. In each penetration, the receptive field positions varied considerably on the same finger or encompassed more than one finger. Although neurons of the same submodality, either skin or deep tended to be set in an array, the most adequate stimulus could vary among neurons of a given array. The variability in the receptive field positions or the most adequate stimuli remained constant irrespective of the angle of the electrode penetration in the cortex. The results are compatible with the idea that vertically arranged neuronal array receive inputs of multiple sources, both thalamacortical and corticocortical, so that interactions between different inputs can readilly occur.Supported by grants from the Japanese Ministry of Education     

Converging patterns of inputs from oral structures in the postcentral somatosensory cortex of conscious macaque monkeys

Single neuronal activities were recorded in the oral region of the postcentral gyrus in conscious Japanese monkeys. Among 5,756 neurons isolated, receptive fields (RFs) and submodalities were identified in 1,502 neurons in area 3b, 970 in area 1, and 1,461 in area 2. The relative incidence of neurons that had bilateral RFs increased gradually upon moving caudally from area 3b to area 2 (bilateral integration). A total of 276 neurons had bimaxillary RFs covering both the maxillary and mandibular divisions of the trigeminal nerve, such as the upper and lower lips, upper and lower teeth, palate and tongue, or combinations thereof. There was also a tendency for the relative incidence of neurons with bimaxillary RFs to increase across the postcentral gyrus but with an abrupt change in area 2 (bimaxillary integration). A total of 382 neurons had composite RFs covering more than one of five oral structures: lip, cheek mucosa, teeth/gingiva, tongue, and palate. The relative incidence of neurons with composite RFs was significantly higher in area 2 than in areas 3b and 1 (interstructural integration). These results indicate that the convergence of inputs from oral structures proceeds in a hierarchical manner across the postcentral gyrus, but chiefly in area 2 for the bimaxillary and interstructural integrations. The relative incidence of neurons with composite RFs was higher among neurons associated with the teeth/gingiva or palate than among neurons associated with the tongue or lip in all three areas. We interpret this to mean that anatomical or functional differences between oral structures might be reflected in the converging patterns in the oral representation.     

Responses of infragranular neurons in the rat primary somatosensory cortex to forepaw and hindpaw tactile stimuli

Infragranular layers constitute the main output of the primary somatosensory cortex and represent an important stage of cortico-cortical and cortico-subcortical integration. We have previously used chronic multiple single-unit recordings to study the spatiotemporal structure of tactile responses of infragranular neurons within the forepaw cortical representation in rats [Tutunculer B, Foffani G, Himes BT, Moxon KA (2006) Structure of the excitatory receptive fields of infragranular forelimb neurons in the rat primary somatosensory cortex responding to touch. Cereb Cortex 16:791-810]. Here we extend our understanding of this structure by studying the overlap between the forepaw and hindpaw cortical representations. We recorded 204 responsive neurons in chronic experiments from eight anesthetized rats. Overall, only 23% of neurons responded exclusively to one paw, 52% of neurons responded to two paws, 19% of neurons responded to three paws, and 5% of neurons responded to all four paws. Quantitative measures of response magnitudes and latencies revealed the following main results. (1) The responses of forepaw neurons overall displayed greater magnitudes and shorter latencies than the responses of hindpaw neurons. (2) The responses to ipsilateral stimuli displayed smaller magnitudes, and longer-and more variable-latencies than the responses to contralateral stimuli. (3) The responses of forepaw neurons to hindpaw stimuli displayed smaller magnitudes and longer latencies than the responses to forepaw stimuli, whereas the responses of hindpaw neurons to forepaw stimuli displayed smaller magnitudes but similar latencies compared with the responses to hindpaw stimuli. These results show that the spatiotemporal structure of tactile responses of infragranular neurons extends across all four paws, and provide the basic architecture for studying physiological integration and pathophysiological reorganization of tactile information in the infragranular layers of the rat primary somatosensory cortex.     

Role of cortical feedback in the receptive field structure and nonlinear response properties of somatosensory thalamic neurons

Previous studies have suggested that the descending pathway from the primary somatosensory (SI) cortex to the ventral posterior nucleus of the thalamus has only a mild facilitative influence over thalamic neurons. Given the large numbers of corticothalamic terminations within the rat somatosensory thalamus and their complex topography, we sought to examine the role of corticothalamic feedback in the genesis of spatiotemporal receptive fields and the integration of complex tactile stimuli in the thalamus. By combining focal cortical inactivation (produced by microinjection of the GABA(A) agonist muscimol), with chronic multielectrode recordings, we observed that feedback from the rat SI cortex has multiple influences on its primary thalamic relay, the ventral posterior medial (VPM) nucleus. Our data demonstrate that, when single-whisker stimuli were used, the elimination of cortical feedback caused significant changes in the spatiotemporal structure of the receptive fields of VPM neurons. Cortical feedback also accounted for the nonlinear summation of VPM neural responses to simultaneously stimulated whiskers, in effect "linearizing" the responses. These results argue that the integration and transmission of tactile information through VPM are strongly influenced by the state of SI cortex.     

Representation of the visual field in the lateral intraparietal area of macaque monkeys: a quantitative receptive field analysis

The representation of the visual field in the primate lateral intraparietal area (LIP) was examined, using a rapid, computer-driven receptive field (RF) mapping procedure. RF characteristics of single LIP neurons could thus be measured repeatedly under different behavioral conditions. Here we report data obtained using a standard ocular fixation task during which the animals were required to monitor small changes in color of the fixated target. In a first step, statistical analyses were conducted in order to establish the experimental limits of the mapping procedure on 171 LIP neurons recorded from three hemispheres of two macaque monkeys. The characteristics of the receptive fields of LIP neurons were analyzed at the single cell and at the population level. Although for many neurons the assumption of a simple two-dimensional gaussian profile with a central area of maximal excitability at the center and progressively decreasing response strength at the periphery can represent relatively accurately the spatial structure of the RF, about 19% of the cells had a markedly asymmetrical shape. At the population level, we observed, in agreement with prior studies, a systematic relation between RF size and eccentricity. However, we also found a more accentuated overrepresentation of the central visual field than had been previously reported and no marked differences between the upper and lower visual representation of space. This observation correlates with an extension of the definition of LIP from the posterior third of the lateral intraparietal sulcus to most of the middle and posterior thirds. Detailed histological analyses of the recorded hemispheres suggest that there exists, in this newly defined unitary functional cortical area, a coarse but systematic topographical organization in area LIP that supports the distinction between its dorsal and ventral regions, LIPd and LIPv, respectively. Paralleling the physiological data, the central visual field is mostly represented in the middle dorsal region and the visual periphery more ventral and posterior. An anteroposterior gradient from the lower to the upper visual field representations can also be identified. In conclusion, this study provides the basis for a reliable mapping method in awake monkeys and a reference for the organization of the properties of the visual space representation in an area LIP extended with respect to the previously described LIP and showing a relative emphasis of central visual field. Electronic Publication     

The effects of aging on the strength of surround suppression of receptive field of V1 cells in monkeys

The surround suppression of the receptive field is important for basic visual information processing, such as orientation specificity. To date, the effects of aging on the strength of surround suppression are not clear. To address this issue, we carried out extracellular single-unit studies of the receptive field properties of cells in the primary visual cortex (area V1) in young and old rhesus (Macaca mulatta) monkeys. When presented with the oriented central stimulus, we found that cells in old animals showed reduced orientation and direction selectivity compared with those in young animals. When presented with the oriented central stimulus together with the optimal surround stimulus, more selective cells {orientation bias (OB) ≥0.1; a bias of 0.1 is significant at the P<0.005 level} in animals of both ages showed reduced orientation selectivity compared with the experiment that presented only the oriented central stimulus. When presented with the optimal central stimulus together with the oriented surround stimulus, cells in old animals showed reduced orientation and direction selectivity compared with young animals. Moreover, broadly tuned cells (OB<0.1) in old animals exhibited significantly reduced suppression indices that quantified the strength of the surround suppression of the receptive field, when compared with those in young animals. These results suggest that aging may seriously affect the surround suppression of the receptive field of V1 cells. Thus, the decreased strength of surround suppression of the receptive field may be one possible reason for the decreased stimulus selectivity of V1 cells previously found in the senescent brain. This work will contribute to an understanding of the physiological mechanisms mediating surround suppression of the receptive field.     

Efferent neurons and suspected interneurons in second somatosensory cortex of the awake rabbit: receptive fields and axonal properties.

1. Receptive-field properties of antidromically identified efferent neurons within the representation of vibrissae and sinus hairs above the mouth were examined in secondary somatosensory cortex (S-2) of fully awake adult rabbits. Efferent neurons studied included callosal neurons (CC neurons, n = 88), ipsilateral corticocortical neurons (C-IC neurons, n = 51) that project to primary somatosensory cortex (S-1), and corticofugal neurons of layer 5 (CF-5 neurons, n = 63) and layer 6 (CF-6 neurons, n = 42) that project to and/or beyond the thalamus. Appropriate collision tests demonstrated that substantial numbers of corticocortical efferent neurons (21 of 113 tested) project an axon to both the corpus callosum and to ipsilateral S-1. 2. Suspected interneurons (SINs, n = 62) were also studied. These neurons were not activated antidromically from any stimulus site but did respond synaptically to electrical stimulation of the ventrobasal (VB) thalamus with a burst of three or more spikes at frequencies of 600 to greater than 900 Hz. Most of these neurons also responded synaptically to stimulation of S-1 and the corpus callosum. The action potentials of these neurons were much shorter (mean, 0.49 ms) than those of efferent neurons (mean, 1.01 ms). 3. CF-5 neurons differed from CC, C-IC, and CF-6 neurons in their spontaneous firing rates, axonal properties, and receptive-field properties. Whereas CF-5 neurons had a mean spontaneous firing rate of 5.7 spikes/s, CC, C-IC, and CF-6 neurons all had mean values of less than 1/s. Axonal conduction velocities of CF-5 neurons were much higher (mean, 11.90 m/s) than either CC (mean, 2.63 m/s), C-IC (mean, 0.86 m/s), or CF-6 (mean, 1.73 m/s) neurons. A decrease in antidromic latency (the "supernormal" period), which was dependent on prior impulse activity, was seen in most CC, C-IC, and CF-6 neurons but was minimal or absent in CF-5 neurons of comparable conduction velocity. Although all CF-5 neurons responded to peripheral sensory stimulation, many CC (52%), C-IC (49%), and CF-6 (55%) neurons did not. CC and CF-6 neurons that did not respond to sensory stimulation had significantly lower axonal conduction velocities and spontaneous firing rates than those that responded to such stimulation. Whereas no CC, C-IC, or CF-6 neuron responded synaptically to callosal stimulation, 43% of CF-5 neurons (and 78% of SINs) did so respond. Similar differences in synaptic responsivity to stimulation of S-1 were seen in these populations.(ABSTRACT TRUNCATED AT 400 WORDS)     

The neural basis of the behaviorally relevant N1 component of the somatosensory-evoked potential in SI cortex of awake monkeys: evidence that backward cortical projections signal conscious touch sensation

Summary Studies of touch intensity discrimination in monkeys have identified a component of the somatosensory-evoked cortical potential, N1, generated within 50 ms of the stimulus, that predicts their behavioral performance. This study employed multiple-electrode arrays with relatively high spatial resolution (0.1 or 0.2 mm spacing) to record laminar profiles of somatosensory-evoked potentials (SEPs), multiple unit activity (MUA) and current source-densities (CSDs) at several sites across the postcentral gyri of two awake monkeys. This high resolution laminar analysis strongly supports our earlier hypothesis based upon low resolution data that N1 is generated by synaptic excitation targeted specifically at the most superficial cortical layers I/II: (1) The excitatory nature of N1 was indicated by elevated MUA which was maximal in layer III and extended down to subcortical white matter where fiber activity exceeded prestimulus levels; (2) In addition to CSD analysis, the observation that N1 was maximally negative within 0.10 mm of the border between layers I and II verified the superficial site of N1 synaptic excitation regardless of conductivity boundaries near the pial surface. A review of the anatomical literature finds that the most likely inputs responsible for N1 activation are the backward cortico-cortical projections from secondary somatosensory areas to SI which in area 1 are the major source of sensory-related input that specifically terminates in layers I/II. We suggest, therefore, that backward projections are involved in the conscious process of touch sensation as it is signaled by N1.