scholarly journals Structure of the Excitatory Receptive Fields of Infragranular Forelimb Neurons in the Rat Primary Somatosensory Cortex Responding To Touch

2005 ◽  
Vol 16 (6) ◽  
pp. 791-810 ◽  
Author(s):  
Banu Tutunculer ◽  
Guglielmo Foffani ◽  
B. Timothy Himes ◽  
Karen A. Moxon
1998 ◽  
Vol 80 (6) ◽  
pp. 2882-2892 ◽  
Author(s):  
Christopher I. Moore ◽  
Sacha B. Nelson

Moore, Christopher I. and Sacha B. Nelson. Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J. Neurophysiol. 80: 2882–2892, 1998. Whole cell recordings of synaptic responses evoked by deflection of individual vibrissa were obtained from neurons within adult rat primary somatosensory cortex. To define the spatial and temporal properties of subthreshold receptive fields, the spread, amplitude, latency to onset, rise time to half peak amplitude, and the balance of excitation and inhibition of subthreshold input were quantified. The convergence of information onto single neurons was found to be extensive: inputs were consistently evoked by vibrissa one- and two-away from the vibrissa that evoked the largest response (the “primary vibrissa”). Latency to onset, rise time, and the incidence and strength of inhibitory postsynaptic potentials (IPSPs) varied as a function of position within the receptive field and the strength of evoked excitatory input. Nonprimary vibrissae evoked smaller amplitude subthreshold responses [primary vibrissa, 9.1 ± 0.84 (SE) mV, n = 14; 1-away, 5.1 ± 0.5 mV, n = 38; 2-away, 3.7 ± 0.59 mV, n = 22; 3-away, 1.3 ± 0.70 mV, n = 8] with longer latencies (primary vibrissa, 10.8 ± 0.80 ms; 1-away, 15.0 ± 1.2 ms; 2-away, 15.7 ± 2.0 ms). Rise times were significantly faster for inputs that could evoke action potential responses (suprathreshold, 4.1 ± 1.3 ms, n = 8; subthreshold, 12.4 ± 1.5 ms, n = 61). In a subset of cells, sensory evoked IPSPs were examined by deflecting vibrissa during injection of hyperpolarizing and depolarizing current. The strongest IPSPs were evoked by the primary vibrissa ( n = 5/5), but smaller IPSPs also were evoked by nonprimary vibrissae ( n = 8/13). Inhibition peaked by 10–20 ms after the onset of the fastest excitatory input to the cortex. This pattern of inhibitory activity led to a functional reversal of the center of the receptive field and to suppression of later-arriving and slower-rising nonprimary inputs. Together, these data demonstrate that subthreshold receptive fields are on average large, and the spatio-temporal dynamics of these receptive fields vary as a function of position within the receptive field and strength of excitatory input. These findings constrain models of suprathreshold receptive field generation, multivibrissa interactions, and cortical plasticity.


2008 ◽  
Vol 100 (1) ◽  
pp. 268-280 ◽  
Author(s):  
Guglielmo Foffani ◽  
John K. Chapin ◽  
Karen A. Moxon

Computational studies are challenging the intuitive view that neurons with broad tuning curves are necessarily less discriminative than neurons with sharp tuning curves. In the context of somatosensory processing, broad tuning curves are equivalent to large receptive fields. To clarify the computational role of large receptive fields for cortical processing of somatosensory information, we recorded ensembles of single neurons from the infragranular forelimb/forepaw region of the rat primary somatosensory cortex while tactile stimuli were separately delivered to different locations on the forelimbs/forepaws under light anesthesia. We specifically adopted the perspective of individual columns/segregates receiving inputs from multiple body location. Using single-trial analyses of many single-neuron responses, we obtained two main results. 1) The responses of even small populations of neurons recorded from within the same estimated column/segregate can be used to discriminate between stimuli delivered to different surround locations in the excitatory receptive fields. 2) The temporal precision of surround responses is sufficiently high for spike timing to add information over spike count in the discrimination between surround locations. This surround spike-timing code (i) is particularly informative when spike count is ambiguous, e.g., in the discrimination between close locations or when receptive fields are large, (ii) becomes progressively more informative as the number of neurons increases, (iii) is a first-spike code, and (iv) is not limited by the assumption that the time of stimulus onset is known. These results suggest that even though large receptive fields result in a loss of spatial selectivity of single neurons, they can provide as a counterpart a sophisticated temporal code based on latency differences in large populations of neurons without necessarily sacrificing basic information about stimulus location.


2000 ◽  
Vol 84 (2) ◽  
pp. 719-729 ◽  
Author(s):  
Dan R. Kenshalo ◽  
Koichi Iwata ◽  
Maurice Sholas ◽  
David A. Thomas

The organization and response properties of nociceptive neurons in area 1 of the primary somatosensory cortex (SI) of anesthetized monkeys were examined. The receptive fields of nociceptive neurons were classified as either wide-dynamic-range (WDR) neurons that were preferentially responsive to noxious mechanical stimulation, or nociceptive specific (NS) that were responsive to only noxious stimuli. The cortical locations and the responses of the two classes of neurons were compared. An examination of the neuronal stimulus-response functions obtained during noxious thermal stimulation of the glabrous skin of the foot or the hand indicated that WDR neurons exhibited significantly greater sensitivity to noxious thermal stimuli than did NS neurons. The receptive fields of WDR neurons were significantly larger than the receptive fields of NS neurons. Nociceptive SI neurons were somatotopically organized. Nociceptive neurons with receptive fields on the foot were located more medial in area 1 of SI than those with receptive fields on the hand. In the foot representation, the recording sites of nociceptive neurons were near the boundary between areas 3b and 1, whereas in the hand area, there was a tendency for them to be located more caudal in area 1. The majority of nociceptive neurons were located in the middle layers (III and IV) of area 1. The fact that nociceptive neurons were not evenly distributed across the layers of area 1 suggested that columns of nociceptive neurons probably do not exist in the somatosensory cortex. In electrode tracks where nociceptive neurons were found, approximately half of all subsequently isolated neurons were also classified as nociceptive. Low-threshold mechanoreceptive (LTM) neurons were intermingled with nociceptive neurons. Both WDR and NS neurons were found in close proximity to one another. In instances where the receptive field shifted, subsequently isolated cells were also classified as nociceptive. These data suggest that nociceptive neurons in area 1 of SI are organized in vertically orientated aggregations or clusters in layers III and IV.


1998 ◽  
Vol 79 (4) ◽  
pp. 2119-2148 ◽  
Author(s):  
Christian Xerri ◽  
Michael M. Merzenich ◽  
Bret E. Peterson ◽  
William Jenkins

Xerri, Christian, Michael M. Merzenich, Bret E. Peterson, and William Jenkins. Plasticity of primary somatosensory cortex paralleling sensorimotor skill recovery from stroke in adult monkeys. J. Neurophysiol. 79: 2119–2148, 1998. Adult owl and squirrel monkeys were trained to master a small-object retrieval sensorimotor skill. Behavioral observations along with positive changes in the cortical area 3b representations of specific skin surfaces implicated specific glabrous finger inputs as important contributors to skill acquisition. The area 3b zones over which behaviorally important surfaces were represented were destroyed by microlesions, which resulted in a degradation of movements that had been developed in the earlier skill acquisition. Monkeys were then retrained at the same behavioral task. They could initially perform it reasonably well using the stereotyped movements that they had learned in prelesion training, although they acted as if key finger surfaces were insensate. However, monkeys soon initiated alternative strategies for small object retrieval that resulted in a performance drop. Over several- to many-week-long period, monkeys again used the fingers for object retrieval that had been used successfully before the lesion, and reacquired the sensorimotor skill. Detailed maps of the representations of the hands in SI somatosensory cortical fields 3b, 3a, and 1 were derived after postlesion functional recovery. Control maps were derived in the same hemispheres before lesions, and in opposite hemispheres. Among other findings, these studies revealed the following 1) there was a postlesion reemergence of the representation of the fingertips engaged in the behavior in novel locations in area 3b in two of five monkeys and a less substantial change in the representation of the hand in the intact parts of area 3b in three of five monkeys. 2) There was a striking emergence of a new representation of the cutaneous fingertips in area 3a in four of five monkeys, predominantly within zones that had formerly been excited only by proprioceptive inputs. This new cutaneous fingertip representation disproportionately represented behaviorally crucial fingertips. 3) There was an approximately two times enlargement of the representation of the fingers recorded in cortical area 1 in postlesion monkeys. The specific finger surfaces employed in small-object retrieval were differentially enlarged in representation. 4) Multiple-digit receptive fields were recorded at a majority of emergent, cutaneous area 3a sites in all monkeys and at a substantial number of area 1 sites in three of five postlesion monkeys. Such fields were uncommon in area 1 in control maps. 5) Single receptive fields and the component fields of multiple-digit fields in postlesion representations were within normal receptive field size ranges. 6) No significant changes were recorded in the SI hand representations in the opposite (untrained, intact) control hemisphere. These findings are consistent with “substitution” and “vicariation” (adaptive plasticity) models of recovery from brain damage and stroke.


2010 ◽  
Vol 104 (6) ◽  
pp. 3136-3145 ◽  
Author(s):  
Jamie L. Reed ◽  
Hui-Xin Qi ◽  
Pierre Pouget ◽  
Mark J. Burish ◽  
A. B. Bonds ◽  
...  

Neurons in the hand representation of primary somatosensory cortex (area 3b) are known to have discretely localized receptive fields; and these neurons form modules that can be visualized histologically as distinct digit and palm representations. Despite these indicators of the importance of local processing in area 3b, widespread interactions between stimuli presented to locations across the hand have been reported. We investigated the relationship of neuron firing rate with distance from the site of maximum activation in cortex by recording from a 100-electrode array with electrodes spaced 400 μm apart, implanted into the area 3b hand representation in anesthetized owl monkeys. For each stimulated location on the hand, the electrode site where neurons had the highest peak firing rate was defined as the peak activation site. The lesser firing rates of neurons at all other electrode sites in the grid were compared with the firing rates of neurons at the peak activation site. On average, peak firing rates of neurons decreased rapidly with distance away from the peak activation site. The effect of distance on the variance of firing rates was highly significant ( P < 0.0001). However, individual neurons retained high firing rates for distances over 3 mm. The clear decline in firing rate with distance from the most activated location indicates that local processing is emphasized in area 3b, while the distance of neurons with reduced but maintained firing rates ≤3–4 mm from the site of best activation demonstrated widespread activation in primary somatosensory cortex.


1991 ◽  
Vol 65 (2) ◽  
pp. 178-187 ◽  
Author(s):  
M. B. Calford ◽  
R. Tweedale

1. Acute effects of permanent and temporary denervation of the flying fox thumb were examined to test the hypothesis that a large area of skin around the cutaneous receptive field of multiunits (MRF) at a locus in primary somatosensory cortex (SI) supplies viable inputs which can be rapidly unmasked by interruption of the dominant input from the area of the MRF. 2. The immediate effect of amputation of the thumb at loci where the original receptive field was entirely removed was to produce large MRFs on adjacent body areas (wrist, forearm, prowing, and finger membranes). Greatly expanded MRFs were also produced when amputation removed only part of the original MRF at a cortical locus. 3. The probable source of input to account for the new receptive fields is the extensive arborization of ascending projections within the somatosensory pathway, which supply a cortical locus with a potential input from a far larger area than is represented in its normal receptive field. The rapidity with which new or expanded fields are seen following denervation indicates that the normally unexpressed inputs around a receptive field are not only potential inputs but are inherently viable. Hence the most likely explanation for the results of this study is that the effect of the denervation is to disrupt an inhibitory influence that normally has the role of shaping the receptive field. 4. Temporary anesthesia of all or part of a MRF produced similar initial effects to amputation. When responsiveness returned to the locally anesthetized area (after 10-30 min), an expanded MRF persisted for a short time after which the boundaries of the MRF shrank. This rapid reversal suggests that a mechanistic rather than a plastic change is the basis for the acute effect of a small denervation on SI.


1992 ◽  
Vol 67 (1) ◽  
pp. 37-63 ◽  
Author(s):  
E. P. Gardner ◽  
C. I. Palmer ◽  
H. A. Hamalainen ◽  
S. Warren

1. To assess the mechanisms used by cortical neurons to sense motion across the skin, we applied pulsatile stimuli to a series of adjacent positions on the glabrous skin of the hand using a computer-controlled OPTACON stimulator. We describe responses of 129 single neurons in primary somatosensory cortex of alert monkeys to a horizontal bar pattern that was displaced proximally or distally in 1.2-mm steps at 10-, 20-, and 40-ms intervals (100, 50, and 25 Hz, respectively). These frequencies span the range in which apparent motion is transformed perceptually in humans from a smooth uninterrupted sweep into a series of distinct pulses that are resolved as separate events. The experiments are thus designed to decipher the neural correlates distinguishing continuous motion from discrete taps. 2. Cortical receptive fields mapped with moving bar patterns spanned 5-24 rows on the tactile array (16.2 +/- 5.4, mean +/- SD). Over 40% of the fields encompassed 18 or more rows (greater than or equal to 21.6 mm), allowing these neurons to integrate spatial information from an entire image displayed on the OPTACON. Cortical receptive fields are considerably larger than those of mechanoreceptors mapped with the same moving bar patterns (4.2 +/- 2.3 rows, mean +/- SD), reflecting convergent inputs in subcortical and cortical relays. Responses were either relatively uniform across the field or strongest at the initial point of entry, depending on the frequency of stimulation. A sharply defined field center was absent from most of the cells recorded in this study. 3. Temporal frequency of stimulation appears to be a major determinant of cortical firing patterns. Low-frequency stimuli are more effective in activating cortical neurons, producing more spikes per sweep and greater phase-locking to individual stimuli than do high frequencies. The total spike output of cortical neurons is proportional to the pulse interval over the range 10-40 ms, increasing linearly by an average of 5.9 spikes/10-ms increase in pulse period. Peak firing rates and modulation amplitude are also highest when pulses are presented at long intervals, falling significantly as the stimulation frequency rises. The reduction in firing at high pulse rates is apparently due to central mechanisms, as both rapidly adapting and Pacinian corpuscle afferents display nearly constant spike outputs and uniform sensitivity within the field when tested with identical bar patterns. Central networks thus behave as low-pass filters, reducing cortical responses to rapidly applied sequential stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)


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