Vagal Input to Lateral Area 3a in Cat Cortex

2003 ◽  
Vol 90 (1) ◽  
pp. 143-154 ◽  
Author(s):  
Shin-Ichi Ito ◽  
A. D. (Bud) Craig

Penfield's sensory homunculus included visceral organs at its lateral extreme, and vagal input was recently identified lateral to the intraoral representation in primary somatosensory cortex (S1) of rats. We tested whether vagal input is similarly located in cats where area 3b (equivalent to S1) is clearly distinguishable from adjacent regions. Field potentials were recorded from the intact dura over the left hemisphere using electrical stimulation of the left or right cervical vagus nerve in seven cats. A surface positive-negative potential was evoked from either side in the lateral part of the sigmoid gyrus. Finer mapping made at the pial surface with a microelectrode identified a focal site anteromedial to the anterior tip of the coronal sulcus. Depth recordings demonstrated polarity reversals and multi-unit vagal responses, indicating that the potentials were generated by an afferent activation focus in the middle layers of the cortex. The S1 mechanoreceptive representation was localized by mapping multi-unit somatosensory receptive fields in the middle cortical layers near the coronal sulcus. The vagal-evoked potential site was distinctly anterior to the intraoral S1 representation and adjacent to the masseteric-nerve-evoked potential focus. Lesions made at the focal site revealed that this site is cytoarchitectonically located in area 3a not area 3b. Thus vagal input to the sensorimotor cortex in cats resembles deep rather than cutaneous somatic input, similar to the localization of nociceptive-specific input to area 3a in monkeys. The possibilities are considered that this vagal input is involved in motor control and in the sensory experience of visceral afferent activity.

1992 ◽  
Vol 68 (2) ◽  
pp. 518-527 ◽  
Author(s):  
T. P. Pons ◽  
P. E. Garraghty ◽  
M. Mishkin

1. Selective ablations of the hand representations in postcentral cortical areas 3a, 3b, 1, and 2 were made in different combinations to determine each area's contribution to the responsivity and modality properties of neurons in the hand representation in SII. 2. Ablations that left intact only the postcentral areas that process predominantly cutaneous inputs (i.e., areas 3b and 1) yielded SII recording sites responsive to cutaneous stimulation and none driven exclusively by high-intensity or "deep" stimulation. Conversely, ablations that left intact only the postcentral areas that process predominantly deep receptor inputs (i.e., areas 3a and 2) yielded mostly SII recording sites that responded exclusively to deep stimulation. 3. Ablations that left intact only area 3a or only area 2 yielded substantial and roughly equal reductions in the number of deep receptive fields in SII. By contrast, ablations that left intact only area 3b or only area 1 yielded unequal reductions in the number of cutaneous receptive fields in SII: a small reduction when area 3b alone was intact but a somewhat larger one when only area 1 was intact. 4. Finally, when the hand representation in area 3b was ablated, leaving areas 3a, 1, and 2 fully intact, there was again a substantial reduction in the encounter rate of cutaneous receptive fields. 5. The partial ablations often led to unresponsive sites in the SII hand representation. In SII representations other than of the hand no such unresponsive sites were found and there were no substantial changes in the ratio of cutaneous to deep receptive fields, indicating that the foregoing results were not due to long-lasting postsurgical depression or effects of anesthesia. 6. The findings indicate that modality-specific information is relayed from postcentral cortical areas to SII along parallel channels, with cutaneous inputs transmitted via areas 3b and 1, and deep inputs via areas 3a and 2. Further, area 3b provides the major source of cutaneous input to SII, directly and perhaps also via area 1. 7. The results are in line with accumulating anatomic and electrophysiologic evidence pointing to an evolutionary shift in the organization of the somatosensory system from the general mammalian plan, in which tactile information is processed in parallel in SI and SII, to a new organization in higher primates in which the processing of tactile information proceeds serially from SI to SII. The presumed functional advantages of this evolutionary shift are unknown.


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.


2015 ◽  
Vol 114 (6) ◽  
pp. 3076-3096 ◽  
Author(s):  
Ryan M. Peters ◽  
Phillip Staibano ◽  
Daniel Goldreich

The ability to resolve the orientation of edges is crucial to daily tactile and sensorimotor function, yet the means by which edge perception occurs is not well understood. Primate cortical area 3b neurons have diverse receptive field (RF) spatial structures that may participate in edge orientation perception. We evaluated five candidate RF models for macaque area 3b neurons, previously recorded while an oriented bar contacted the monkey's fingertip. We used a Bayesian classifier to assign each neuron a best-fit RF structure. We generated predictions for human performance by implementing an ideal observer that optimally decoded stimulus-evoked spike counts in the model neurons. The ideal observer predicted a saturating reduction in bar orientation discrimination threshold with increasing bar length. We tested 24 humans on an automated, precision-controlled bar orientation discrimination task and observed performance consistent with that predicted. We next queried the ideal observer to discover the RF structure and number of cortical neurons that best matched each participant's performance. Human perception was matched with a median of 24 model neurons firing throughout a 1-s period. The 10 lowest-performing participants were fit with RFs lacking inhibitory sidebands, whereas 12 of the 14 higher-performing participants were fit with RFs containing inhibitory sidebands. Participants whose discrimination improved as bar length increased to 10 mm were fit with longer RFs; those who performed well on the 2-mm bar, with narrower RFs. These results suggest plausible RF features and computational strategies underlying tactile spatial perception and may have implications for perceptual learning.


1989 ◽  
Vol 62 (3) ◽  
pp. 778-788 ◽  
Author(s):  
W. S. Ammons

1. Experiments were performed to examine responses of spinothalamic tract (STT) neurons to distension of the renal pelvis. Nineteen monkeys (Macaca fascicularis) were anesthetized with alpha-chloralose, paralyzed, and artificially ventilated. Fifty-four STT neurons in the T11-L2 segments were studied. Each cell was excited by renal nerve stimulation and had a somatic receptive field in the left flank and/or the abdomen. 2. Distension of the left renal pelvis to 50 mmHg for 20-30 s increased activity of 40 STT neurons. Two types of responses were observed. Six cells responded rapidly to the increase in renal pelvic pressure. Thereafter activity of these cells completely adapted. The other 34 cells also responded rapidly to the distension: however, the subsequent adaptation was not complete. Average activity before distension was 13 +/- 1 (SE) spikes/s. Distension increased activity to a peak of 42 +/- 3 spikes/s. Mean activity just before the end of the distension was 27 +/- 3 spikes/s. 3. The pelvic pressure-cell response relation was determined for 16 cells. Only one cell responded to a pressure of 20 mmHg. Three responded to 30 mmHg, and all others responded to 40 mmHg and higher. The average response threshold was 32 +/- 1 mmHg. Peak responses increased as distending pressure increased from 40-80 mmHg. Responses to a pressure of 100 mmHg were no greater than to 80 mmHg. Adapted levels of activity were also a function of distending pressure in the 40-80 mmHg range. 4. Probability of responses was unrelated to somatic input. However, cells with A delta- and C-fiber renal input were significantly more likely to respond to renal pelvic distension than cells with only A delta-renal input. Magnitude of responses to a pressure of 50 mmHg was not related to the type of renal input to the cells; however, among the cells tested at all pressures, cells with A delta- and C-fiber input had significantly greater responses to pressures of 80 and 100 mmHg. 5. Cells were studied in laminae I and IV-VII: responses were unrelated to laminar location. None of the 6 cells located in L2 responded to renal pelvic distension; 8 of 12 in L1 responded; 24 of 28 in T12 responded; and all 8 cells in T11 responded. 6. Stimulation of inhibitory receptive fields on the right hindlimb reduced activity of four cells to a significantly greater extent during pelvic distension than before pelvic distension.(ABSTRACT TRUNCATED AT 400 WORDS)


1988 ◽  
Vol 60 (6) ◽  
pp. 1967-1981 ◽  
Author(s):  
W. S. Ammons

1. Studies were done to characterize responses of spinal neurons backfired from the ventrolateral medulla to renal and somatic stimuli. Experiments were performed on 31 cats that were anesthetized with alpha-chloralose. Sixty-six spinal neurons were antidromically activated from the area of the lateral reticular nucleus or the ventrolateral reticular formation just rostral to the lateral reticular nucleus contralateral to the recording site. These cells could not be backfired from the medial reticular formation or from the spinothalamic tract just caudal to the thalamus. 2. Cells were located in laminae I, V, and VII of the T12-L2 segments. Antidromic conduction velocities averaged 35.9 +/- 7.2 m/s. Conduction velocities were unrelated to the projection site or laminar location of the cells. Termination sites of 21 cells were located in antidromic mapping experiments. Terminals were localized to the ventrolateral reticular formation, including the lateral reticular nucleus. 3. Responses to electrical stimulation of the renal nerves were always excitatory. Stimulation of renal A-delta-fibers excited 33 cells. These cells failed to respond to stimulation of renal C-fibers. The other 33 cells responded to both A-delta- and C-fiber stimulation. Latencies to A-delta-fiber stimulation averaged 9 +/- 2 ms, whereas latencies to C-fiber stimulation averaged 57 +/- 10 ms. 4. Renal mechanoreceptors were activated by occlusion of the renal vein or upper portion of the ureter. Renal vein occlusion excited 14 of 32 cells tested. Activity increased from 6 +/- 2 to 14 +/- 4 spike/s. Ureteral occlusion increased activity of 19 of 32 cells from 7 +/- 2 to 16 +/- 5 spikes/s. Cells responding to one of the mechanical stimuli were significantly more likely to receive A-delta-and C-fiber input compared with nonresponding cells. Nonresponders were more likely than responders to receive only A-delta input. 5. All cells received somatic input in addition to renal input. Twelve cells were classified as wide dynamic range, 46 as high threshold, and 8 as Deep. Somatic receptive fields most often included skin and muscle of the left flank and abdomen. Thirty-two cells had bilateral receptive fields, and 22 had inhibitory fields in addition to excitatory fields. 6. These data show that spinal neurons projecting to the ventrolateral medulla receive convergent inputs from the kidney and somatic structures. These cells may participate in a variety of functions including autonomic reflexes of renal origin.


2011 ◽  
Vol 106 (2) ◽  
pp. 722-730 ◽  
Author(s):  
Ulf Baumgärtner ◽  
Hagen Vogel ◽  
Shinji Ohara ◽  
Rolf-Detlef Treede ◽  
Fred Lenz

The cortical potentials evoked by cutaneous application of a laser stimulus (laser evoked potentials, LEP) often include potentials in the primary somatic sensory cortex (S1), which may be located within the subdivisions of S1 including Brodmann areas 3A, 3B, 1, and 2. The precise location of the LEP generator may clarify the pattern of activation of human S1 by painful stimuli. We now test the hypothesis that the generators of the LEP are located in human Brodmann area 1 or 3A within S1. Local field potential (LFP) source analysis of the LEP was obtained from subdural grids over sensorimotor cortex in two patients undergoing epilepsy surgery. The relationship of LEP dipoles was compared with dipoles for somatic sensory potentials evoked by median nerve stimulation (SEP) and recorded in area 3B (see Baumgärtner U, Vogel H, Ohara S, Treede RD, Lenz FA. J Neurophysiol 104: 3029–3041, 2010). Both patients had an early radial dipole in S1. The LEP dipole was located medial, anterior, and deep to the SEP dipole, which suggests a nociceptive dipole in area 3A. One patient had a later tangential dipole with positivity posterior, which is opposite to the orientation of the SEP dipole in area 3B. The reversal of orientations between modalities is consistent with the cortical surface negative orientation resulting from superficial termination of thalamocortical neurons that receive inputs from the spinothalamic tract. Therefore, the present results suggest that the LEP may result in a radial dipole consistent with a generator in area 3A and a putative later tangential generator in area 3B.


1991 ◽  
Vol 66 (3) ◽  
pp. 1048-1058 ◽  
Author(s):  
T. Allard ◽  
S. A. Clark ◽  
W. M. Jenkins ◽  
M. M. Merzenich

1. These experiments were designed to test the hypothesis that temporally correlated afferent input activity plays a lifelong role in the establishment and modification of receptive fields (RFs) and representational topographies in the primary somatosensory cortex of adult monkeys. They were based in part on the finding that adjacent digits of the hand are represented discontinuously in area 3b of the adult owl monkey. If cortical receptive fields and the details of cortical topographic representations are shaped by the weights of the temporal correlations among afferent inputs, then representational discontinuities between digits would be expected to arise because inputs from the skin surfaces of adjacent digits are largely independent in the critical time domain. 2. In the present experiments, the skin of adjacent digits 3 and 4 of the monkey hand was surgically connected to create an artificial syndactyly, or webbed-finger condition. Highly detailed microelectrode maps of the cortical representation of the syndactyl digits were obtained 3-7.5 mo later. This experimental manipulation greatly increased the amount of simultaneous or nearly simultaneous input from the normally separated, now fused, surfaces of adjacent fingers. 3. Cortical maps of the representations of finger surfaces were highly modified from the normal after a several-month-long period of digital fusion. Specifically, the normal discontinuity between the cortical representations of adjacent fingers was abolished. Within a wide cortical zone, RFs were defined that extended across the line of syndactyly onto the surgically joined skin of both fused digits. The representational topography of the fused digits was similar to any normal single digit and was characterized by a continuous progression of partially overlapping RFs. 4. Control observations revealed that these reorganizational changes cannot be accounted for by any changes in cutaneous innervation induced by the surgery. They must arise from representational changes in the central somatosensory system. 5. These findings reveal that cortical maps can be altered in detail in adult monkeys by modifying the distributed temporal structure of afferent inputs. They support the longstanding hypothesis that the temporal coincidence of inputs plays a role in the grouping of input subsets into specific cortical RFs and, consequently, in the shaping of selected effective cortical inputs and representational topographies throughout life.


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