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

1991 ◽  
Vol 66 (4) ◽  
pp. 1392-1409 ◽  
Author(s):  
H. A. Swadlow

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)

1994 ◽  
Vol 71 (2) ◽  
pp. 437-453 ◽  
Author(s):  
H. A. Swadlow

1. Properties of antidromically identified efferent neurons within the cortical representation of the vibrissae, sinus hairs, and philtrum were examined in motor cortex of fully awake adult rabbits. Efferent neurons were tested for both receptive field and axonal properties and included callosal (CC) neurons (n = 31), ipsilateral corticocortical (C-IC) neurons (n = 34) that project to primary somatosensory cortex (S-1), and corticofugal neurons of layer 5 (CF-5) (n = 33) and layer 6 (CF-6) (n = 32) that project to and/or beyond the thalamus. Appropriate collision tests demonstrated that substantial numbers of corticocortical efferent neurons project an axon to both the corpus callosum and to ipsilateral S-1. 2. Suspected interneurons (SINs, n = 37) were also studied. These neurons were not activated antidromically from any stimulus site but did respond synaptically to electrical stimulation of the ventrolateral (VL) thalamus and/or S-1 with a burst of three or more spikes at frequencies from 600 to > 900 Hz. All of these neurons also responded synaptically to stimulation of the corpus callosum. The action potentials of these neurons were much shorter in duration (mean = 0.48 ms), than those of efferent neurons (mean = 0.90 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 4.1 spikes/s, CC, C-IC, and CF-6 neurons all had mean values of < 1 spike/s. Axonal conduction velocities of CF-5 neurons were much higher (mean = 12.76 m/s) than either CC (1.47 m/s), C-IC (0.97 m/s), or CF-6 (mean = 1.96 m/s) neurons. A decrease in antidromic latency (the "supernormal" period) followed a single prior impulse in most CC, C-IC, and CF-6 neurons but was minimal or absent in CF-5 neurons. Although all but two CF-5 neurons responded to peripheral sensory stimulation, many CC (35%), C-IC (59%), or CF-6 (66%) neurons did not. CC, CF-5, 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. 4. Sensory receptive fields of neurons in motor cortex were considerably larger than those observed in S-1 but were similar in size to those seen in secondary somatosensory cortex (S-2).(ABSTRACT TRUNCATED AT 400 WORDS)


1990 ◽  
Vol 63 (6) ◽  
pp. 1477-1498 ◽  
Author(s):  
H. A. Swadlow

1. Receptive-field properties of antidromically identified efferent neurons within the cutaneous forelimb representation of primary somatosensory cortex (S-1) were examined in fully awake rabbits. Efferent neurons studied included callosal neurons (CC neurons, n = 52), ipsilateral corticocortical neurons (C-IC neurons, n = 48) that project to or beyond the second somatosensory cortical area (S-2), and corticofugal neurons of layer 5 (CF-5 neurons, n = 97) and layer 6 (CF-6 neurons, n = 59) that project to and/or beyond the thalamus. 2. An additional class of neurons was studied that was not activated antidromically from any stimulus site, but which responded 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-2 and the corpus callosum. The action potentials of these neurons were much shorter (mean = 0.45 ms) than those of efferent neurons (mean = 0.95 ms). Such properties have been associated with interneurons found throughout the central nervous system, and these neurons are thereby referred to as suspected interneurons (SINs). 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 5.5 spikes/s, CC, C-IC, and CF-6 neurons had mean values of less than 1/s. Axonal conduction velocities of CF-5 neurons were much higher (mean = 12.92 m/s) than either CC (mean = 2.15 m/s), C-IC (mean = 1.31 m/s), or CF-6 (mean = 2.53 m/s) neurons. A decrease in antidromic latency (the "supernormal" period) that was dependent on prior impulse activity was seen in the great majority of CC, C-IC, and CF-6 neurons but was either minimal or absent in CF-5 neurons of comparable conduction velocity. A higher proportion of CF-5 neurons (98%) responded to peripheral sensory stimulation than did either CC (75%), C-IC (71%), or CF-6 (51%) neurons. CF-6 and C-IC 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. 4. Cutaneous receptive fields were seen in most neurons that could be driven by peripheral stimulation.(ABSTRACT TRUNCATED AT 400 WORDS)


1988 ◽  
Vol 59 (4) ◽  
pp. 1162-1187 ◽  
Author(s):  
H. A. Swadlow

1. In fully awake rabbits the stability of the two eyes was monitored and was sufficient to enable receptive-field analysis of antidromically identified efferent neurons and suspected interneurons in the binocular segment of visual area 1. Efferent neurons analyzed included callosal efferent neurons (CC neurons, n = 52), neurons projecting to visual area 2 (CV2 neurons, n = 35), corticotectal neurons (CT neurons, n = 43), and corticogeniculate neurons (CG neurons, n = 51). Six additional neurons projected a branching axon to both the corpus callosum and visual area 2. 2. Most CC and CV2 neurons were found in layer 2-3 and had receptive fields of the simple type. Only two corticocortical neurons with complex receptive fields were found. Orientation tuning ranges of CC and CV2 simple cells were similar and end stopping was prevalent in both CC (62%) and CV2 (45%) neurons. Axonal conduction velocities of CC and CV2 neurons were low (mean = 3.5 and 1.4 m/s, respectively) and visually nonresponsive CC neurons (19%) had conduction velocities that were significantly lower than visually responsive neurons. Spontaneous firing rates of corticocortical neurons were low (mean less than 1 spike/s) and these neurons responded to a lower range of stimulus velocities than did corticofugal neurons. 3. Most CG neurons had simple receptive fields and none had a complex field. Orientation tuning ranges of these neurons were comparable to those of CC and CV2 neurons, but a significantly smaller proportion (12%) were end stopped. Both spontaneous firing rates (mean = less than 1 spike/s) and axonal conduction velocities (mean = 2.4 m/s) of CG neurons were low and, as was found for CC neurons, visually nonresponsive CG neurons (25%) had significantly lower conduction velocities than did visually responsive neurons. 4. CT neurons had receptive fields that were predominantly complex (37%), motion/uniform (28%), or simple (26%). Conduction velocities (mean = 10.9 m/s) and spontaneous firing rates (mean = 7 spikes/s) of CT neurons of all receptive-field types were much higher than those of CC, CV2, and CG neurons. 5. An additional class of neurons was studied that responded synaptically at a short latency to electrical stimulation of the dorsal lateral geniculate nucleus (LGNd) with a burst of three or more spikes at frequencies of 600-900 Hz. These neurons showed a high degree of synaptic convergence, also responding synaptically with a high-frequency burst of spikes to stimulation of both visual area 2 and the corpus callosum.(ABSTRACT TRUNCATED AT 400 WORDS)


1987 ◽  
Vol 57 (4) ◽  
pp. 977-1001 ◽  
Author(s):  
H. A. Swadlow ◽  
T. G. Weyand

The intrinsic stability of the rabbit eye was exploited to enable receptive-field analysis of antidromically identified corticotectal (CT) neurons (n = 101) and corticogeniculate (CG) neurons (n = 124) in visual area I of awake rabbits. Eye position was monitored to within 1/5 degrees. We also studied the receptive-field properties of neurons synaptically activated via electrical stimulation of the dorsal lateral geniculate nucleus (LGNd). Whereas most CT neurons had either complex (59%) or motion/uniform (15%) receptive fields, we also found CT neurons with simple (9%) and concentric (4%) receptive fields. Most complex CT cells were broadly tuned to both stimulus orientation and velocity, but only 41% of these cells were directionally selective. We could elicit no visual responses from 6% of CT cells, and these cells had significantly lower conduction velocities than visually responsive CT cells. The median spontaneous firing rates for all classes of CT neurons were 4-8 spikes/s. CG neurons had primarily simple (60%) and concentric (9%) receptive fields, and none of these cells had complex receptive fields. CG simple cells were more narrowly tuned to both stimulus orientation and velocity than were complex CT cells, and most (85%) were directionally selective. Axonal conduction velocities of CG neurons (mean = 1.2 m/s) were much lower than those of CT neurons (mean = 6.4 m/s), and CG neurons that were visually unresponsive (23%) had lower axonal conduction velocities than did visually responsive CG neurons. Some visually unresponsive CG neurons (14%) responded with saccadic eye movements. The median spontaneous firing rates for all classes of CG neurons were less than 1 spike/s. All neurons synaptically activated via LGNd stimulation at latencies of less than 2.0 ms had receptive fields that were not orientation selective (89% motion/uniform, 11% concentric), whereas most cells with orientation-selective receptive fields had considerably longer synaptic latencies. Most short-latency motion/uniform neurons responded to electrical stimulation of the LGNd (and visual area II) with a high-frequency burst (500-900 Hz) of three or more spikes. Action potentials of these neurons were of short duration, thresholds of synaptic activation were low, and spontaneous firing rates were the highest seen in rabbit visual cortex. These properties are similar to those reported for interneurons in several regions in mammalian central nervous system. Nonvisual sensory stimuli that resulted in electroencephalographic arousal (hippocampal theta activity) had a profound effect on the visual responses of many visual cortical neurons.(ABSTRACT TRUNCATED AT 400 WORDS)


2003 ◽  
Vol 90 (3) ◽  
pp. 1842-1851 ◽  
Author(s):  
Charles P. Pluto ◽  
Richard D. Lane ◽  
Nicolas L. Chiaia ◽  
Andrey S. Stojic ◽  
Robert W. Rhoades

Rats that sustain forelimb removal on postnatal day (P) 0 exhibit numerous multi-unit recording sites in the forelimb-stump representation of primary somatosensory cortex (SI) that also respond to hindlimb stimulation when cortical GABAA+B receptors are blocked. Most of these hindlimb inputs originate in the medial SI hindlimb representation. Although many forelimb-stump sites in these animals respond to hindlimb stimulation, very few respond to stimulation of the face (vibrissae or lower jaw), which is represented in SI just lateral to the forelimb. The lateral to medial development of SI may influence the capacity of hindlimb (but not face) inputs to “invade” the forelimb-stump region in neonatal amputees. The SI forelimb-stump was mapped in adult (>60 days) rats that had sustained amputation on embryonic day (E) 16, on P0, or during adulthood. GABA receptors were blocked and subsequent mapping revealed increases in nonstump inputs in E16 and P0 amputees: fetal amputees exhibited forelimb-stump sites responsive to face (34%), hindlimb (10%), and both (22%); neonatal amputees exhibited 10% face, 39% hindlimb, and 5% both; adult amputees exhibited 10% face, 5% hindlimb, and 0% both, with ∼80% stump-only sites. These results indicate age-dependent differences in receptive-field reorganization of the forelimb-stump representation, which may reflect the spatiotemporal development of SI. Results from cobalt chloride inactivation of the SI vibrissae region and electrolesioning of the dysgranular cortex suggest that normally suppressed vibrissae inputs to the SI forelimb-stump area originate in the SI vibrissae region and synapse in the dysgranular cortex.


2003 ◽  
Vol 90 (3) ◽  
pp. 1556-1570 ◽  
Author(s):  
Brandon S. Minnery ◽  
Randy M. Bruno ◽  
Daniel J. Simons

To understand how the lemniscal trigeminothalamic circuit (PrV → VPM) of the rodent whisker-to-barrel pathway transforms afferent signals, we applied ramp-and-hold deflections to individual whiskers of lightly narcotized rats while recording the extracellular responses of neurons in either the ventroposterior medial (VPM) thalamic nucleus or in brain stem nucleus principalis (PrV). In PrV, only those neurons antidromically determined to project to VPM were selected for recording. We found that VPM neurons exhibited smaller response magnitudes and greater spontaneous firing rates than those of their PrV inputs, but that both populations were similarly well tuned for stimulus direction. In addition, fewer VPM (74%) than PrV neurons (93%) responded with sustained, or tonic, discharges during the plateau phase of the stimulus. Neurons in both populations responded most robustly to deflections of a single, “principal whisker” (PW), and the majority of cells in both PrV (90%) and VPM (73%) also responded to deflections of at least one adjacent whisker (AW). AW responses in both nuclei occurred on average at longer latencies and were more temporally dispersed than PW responses. Lateral inhibition, as evidenced by AW-evoked activity suppression, was rare in PrV but prevalent in VPM. In both nuclei, however, suppression was weak, with AW responses being on average excitatory. Our results suggest that the receptive-field structures and response properties of individual VPM neurons can be explained in large part by input from one or a small number of PrV neurons, but that intrathalamic mechanisms act to further transform the afferent signal.


Author(s):  
W. Schellekens ◽  
M. Thio ◽  
S. Badde ◽  
J. Winawer ◽  
N. Ramsey ◽  
...  

AbstractSeveral neuroimaging studies have shown the somatotopy of body part representations in primary somatosensory cortex (S1), but the functional hierarchy of distinct subregions in human S1 has not been adequately addressed. The current study investigates the functional hierarchy of cyto-architectonically distinct regions, Brodmann areas BA3, BA1, and BA2, in human S1. During functional MRI experiments, we presented participants with vibrotactile stimulation of the fingertips at three different vibration frequencies. Using population Receptive Field (pRF) modeling of the fMRI BOLD activity, we identified the hand region in S1 and the somatotopy of the fingertips. For each voxel, the pRF center indicates the finger that most effectively drives the BOLD signal, and the pRF size measures the spatial somatic pooling of fingertips. We find a systematic relationship of pRF sizes from lower-order areas to higher-order areas. Specifically, we found that pRF sizes are smallest in BA3, increase slightly towards BA1, and are largest in BA2, paralleling the increase in visual receptive field size as one ascends the visual hierarchy. Additionally, we find that the time-to-peak of the hemodynamic response in BA3 is roughly 0.5 s earlier compared to BA1 and BA2, further supporting the notion of a functional hierarchy of subregions in S1. These results were obtained during stimulation of different mechanoreceptors, suggesting that different afferent fibers leading up to S1 feed into the same cortical hierarchy.


1988 ◽  
Vol 59 (4) ◽  
pp. 1231-1252 ◽  
Author(s):  
R. Metherate ◽  
N. Tremblay ◽  
R. W. Dykes

1. Two-hundred thirty-three single neurons were isolated and studied in somatosensory cortex of cats anesthetized with pentobarbital sodium or urethane. Two-hundred and three were studied during iontophoretic administration of acetylcholine (ACh), 173 during administration of glutamate, and 24 during administration of atropine. 2. Fifty-six percent of the 218 neurons tested responded to somatic stimuli. Another 21% did so during glutamate administration. In 11 cases ACh iontophoresis uncovered a receptive field in a previously unresponsive cell. 3. Forty-six percent of the 160 cells tested responded to thalamic stimulation. Another 17% did so in the presence of glutamate, but 19 cells responded to neither cutaneous nor thalamic stimuli. 4. Sixteen percent of the 203 cells tested were overtly excited by ACh and the responses to somatic stimulation of 29% were modulated by administration of ACh. Cells displaying overt excitation and/or modulation of responses were said to be cholinoceptive and made up 39% of the sample. These cells were located in all cortical layers. 5. Cholinoceptive neurons were more likely than noncholinoceptive cells to be driven by thalamic stimulation. 6. The changes observed during ACh administration tended to be facilitatory: an enhanced responsiveness to somatic stimuli, an increased firing rate, or an increased receptive-field size. However, in 10 of the 203 cases tested one or more of these variables decreased. 7. The enhanced responsiveness during ACh administration was a robust phenomenon; responses were often increased by as much as 200% and the discharge pattern was altered so that bursts of impulses following stimulation were more common. 8. ACh tended to enhance one attribute of a cell selectively rather than to act as a general excitant. 9. ACh is a powerful neuromodulatory agent in somatosensory cortex that, when released in specific behavioral states, should enhance the responsiveness of cortical neurons.


2020 ◽  
Vol 123 (3) ◽  
pp. 1072-1089
Author(s):  
Anita Cybulska-Klosowicz ◽  
François Tremblay ◽  
Wan Jiang ◽  
Stéphanie Bourgeon ◽  
El-Mehdi Meftah ◽  
...  

This study compared the receptive field (RF) properties and firing rates of neurons in the cutaneous hand representation of primary somatosensory cortex (areas 3b, 1, and 2) of 9 awake, adult macaques that were intensively trained in a texture discrimination task using active touch (fingertips scanned over the surfaces using a single voluntary movement), passive touch (surfaces displaced under the immobile fingertips), or both active and passive touch. Two control monkeys received passive exposure to the same textures in the context of a visual discrimination task. Training and recording extended over 1–2 yr per animal. All neurons had a cutaneous receptive field (RF) that included the tips of the stimulated digits (D3 and/or D4). In area 3b, RFs were largest in monkeys trained with active touch, smallest in those trained with passive touch, and intermediate in those trained with both; i.e., the mode of touch differentially modified the cortical representation of the stimulated fingers. The same trends were seen in areas 1 and 2, but the changes were not significant, possibly because a second experience-driven influence was seen in areas 1 and 2, but not in area 3b: smaller RFs with passive exposure to irrelevant tactile inputs compared with recordings from one naive hemisphere. We suggest that added feedback during active touch and higher cortical firing rates were responsible for the larger RFs with behavioral training; this influence was tempered by periods of more restricted sensory feedback during passive touch training in the active + passive monkeys. NEW & NOTEWORTHY We studied experience-dependent sensory cortical plasticity in relation to tactile discrimination of texture using active and/or passive touch. We showed that neuronal receptive fields in primary somatosensory cortex, especially area 3b, are largest in monkeys trained with active touch, smallest in those trained with passive touch, and intermediate in those trained using both modes of touch. Prolonged, irrelevant tactile input had the opposite influence in areas 1 and 2, favoring smaller receptive fields.


1997 ◽  
Vol 77 (1) ◽  
pp. 24-42 ◽  
Author(s):  
Steven J. Luck ◽  
Leonardo Chelazzi ◽  
Steven A. Hillyard ◽  
Robert Desimone

Luck, Steven J., Leonardo Chelazzi, Steven A. Hillyard, and Robert Desimone. Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. J. Neurophysiol. 77: 24–42, 1997. Many neurons in extrastriate visual cortex have large receptive fields, and this may lead to significant computational problems whenever multiple stimuli fall within a single field. Previous studies have suggested that when multiple stimuli fall within a cell's receptive field, they compete for the cell's response in a manner that can be biased in favor of attended stimuli. In the present study we examined this role of attention in areas V1, V2, and V4 of macaque monkeys with the use of a behavioral paradigm in which attention was directed to one of two stimulus locations. When two stimuli were presented simultaneously inside the cell's receptive field (which could be accomplished only in areas V2 and V4), we found that the cell's response was strongly influenced by which of the two stimuli was attended. The size of this attention effect was reduced when the attended and ignored stimuli were presented sequentially rather than simultaneously. In addition, the effects became very weak and inconsistent in these areas when only one of the two stimuli was located inside the receptive field. Attention thus modulated sensory responses primarily when two or more simultaneous stimuli competed for access to a neuron's receptive field. As in areas V2 and V4, attention did not modulate sensory responses in area V1 when only a single stimulus was inside the receptive field. In addition, the small receptive fields in this area precluded the simultaneous presentation of attended and ignored stimuli inside the receptive field, making it impossible to determine whether attention effects would be observed under the conditions that led to consistent attention effects in areas V2 and V4. Spontaneous firing rates in areas V2 and V4 were found to be 30–40% higher when attention was directed inside rather than outside the receptive field, even when no stimulus was present in the receptive field. Spontaneous firing rates also varied according to the particular location within the receptive field that was attended. These shifts in spontaneous activity may reflect a top-down signal that biases responses in favor of stimuli at the attended location.


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