Somatosensory, multisensory, and task-related neurons in cortical area 7b (PF) of unanesthetized monkeys

1994 ◽  
Vol 72 (2) ◽  
pp. 542-564 ◽  
Author(s):  
W. K. Dong ◽  
E. H. Chudler ◽  
K. Sugiyama ◽  
V. J. Roberts ◽  
T. Hayashi

1. The goal of this study was to quantitatively characterize the response properties of somatosensory and multisensory neurons in cortical area 7b (or PF) of monkeys that were behaviorally trained to perform an appetitive tolerance-escape task. Particular emphasis was given to characterizing nociceptive thermal responses and correlating such responses to thermal pain tolerance as measured by escape frequency. 2. A total of 244 neurons that responded to somatosensory stimulation alone or to both somatosensory and visual stimulation (multisensory) were isolated and studied in the trigeminal region of cortical area 7b. Thirty neurons responded only to visual stimulation. Thermoreceptive neurons formed approximately 13% (31 of 244) of the neurons that had somatosensory response properties. Thermal nociceptive neurons made up approximately 9% (21 of 244) of the neurons that had somatosensory response properties or approximately 68% (21 of 31) of the neurons that had thermoreceptive response properties. Thermal nociceptive neurons responded either exclusively to noxious thermal stimuli (high-threshold thermoreceptive, HTT) or differentially to nonnoxious and noxious thermal stimuli (wide-range thermoreceptive, WRT). Multimodal HTT neurons had nonnociceptive (low-threshold mechanoreceptive, LTM) and/or nociceptive (nociceptive-specific, wide-dynamic-range) mechanical receptive fields, whereas multimodal WRT neurons had only nonnociceptive (LTM) mechanical receptive fields. Thermal nonnociceptive neurons (low-threshold thermoreceptive, LTT) made up approximately 3% (8 of 244) of the neurons that had somatosensory properties or approximately 26% (8 of 31) of the neurons that were thermoreceptive. The background discharge of two thermoreceptive neurons (6%, 2 of 31) was inhibited by innocuous thermal stimulation. 3. Thermal nociceptive neurons (HTT and WRT) were functionally differentiated by statistical analyses into subpopulations that did encode (HTT-EN, WRT-EN) and did not encode (HTT-NE, WRT-NE) the magnitude of noxious thermal stimulus intensities. The mean slopes and median regression coefficients for the stimulus-response (S-R) functions of HTT-EN and WRT-EN neurons, respectively, were significantly greater than those for the S-R functions of HTT-NE and WRT-NE neurons. In contrast to HTT-NE and WRT-NE neurons, HTT-EN and WRT-EN neurons reliably encoded the magnitude of noxious thermal intensity by grading their mean discharge frequency. 4. The S-R functions of HTT-EN and WRT-EN neurons, unlike those of HTT-NE and WRT-NE neurons, closely approximated stimulus intensity-escape frequency functions.(ABSTRACT TRUNCATED AT 400 WORDS)

1993 ◽  
Vol 69 (2) ◽  
pp. 318-328 ◽  
Author(s):  
D. A. Simone ◽  
M. E. Hanson ◽  
N. A. Bernau ◽  
B. H. Pubols

1. Responses to noxious mechanical and thermal stimuli were examined in 48 thalamic neurons in barbiturate or chloralose-anesthetized raccoons, with special attention to neurons whose peripheral receptive fields (RFs) included glabrous skin of the forepaw. Recording loci were in the core of the ventrobasal complex (VB; n = 32), its ventral or dorsal border (n = 5), or the medial division of the posterior nuclear group (POm; n = 11). 2. Twenty-one VB neurons and 7 POm neurons were classed as wide dynamic range (WDR), whereas 2 VB neurons and 4 POm neurons were classed as nociceptive specific (NS). Response properties of 14 light touch (LT) neurons located in VB were also examined. 3. WDR and NS neurons were not segregated, but rather were intermixed along the ventral and dorsal borders of VB, as well as in POm, and WDR and LT neurons were intermixed in the core of VB. Within the VB core, both LT and WDR neurons were somatotopically organized. 4. All WDR neurons had larger high-threshold than low-threshold RFs, and this difference was greater for POm neurons than for VB neurons. RF areas of LT neurons and low-threshold RF areas of WDR neurons were comparable to those previously reported for raccoon VB units. 5. Out of 25 WDR cells tested, 20 had heat thresholds > 53 degrees C; the range of thresholds in the remaining 5 was 49-53 degrees C. Four out of five NS neurons tested had heat thresholds > 53 degrees C; the threshold of the fifth was 51 degrees C. Of the six neurons with heat thresholds < or = 53 degrees C, two each were in the core of VB, along the border of VB, and in POm. 6. Sensitization to heat after a mild heat injury to the glabrous RF (53 degrees C for 90 s, or 55 degrees C for 30 s) occurred in 8 out of 16 neurons tested, and persisted for up to 2 h. Median thresholds decreased from > 53 degrees C before injury to 47 degrees C after injury, and responses to suprathreshold stimuli were enhanced. There was a significantly greater likelihood (P = 0.02) for sensitization to occur in POm neurons (6/7) than in VB neurons (2/9). 7. It is suggested that a small proportion of neurons located in VB and POm contribute to the sensation of heat pain. Furthermore, sensitization of these neurons may contribute to heat hyperalgesia after an injury to glabrous skin.


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.


1993 ◽  
Vol 69 (6) ◽  
pp. 1890-1903 ◽  
Author(s):  
E. H. Chudler ◽  
K. Sugiyama ◽  
W. K. Dong

1. Extracellular recordings were made from neurons in the neostriatum (caudate nucleus-putamen, CPu) and globus pallidus (GP) of anesthetized rats. Few cells (3%) were classified as low-threshold-mechanoreceptive (LTM) neurons. The majority (97%) of somatosensory CPu and GP neurons responded differentially or exclusively to noxious mechanical stimulation of the skin. Nociceptive neurons were classified into the following three groups on the basis of their response properties to noxious mechanical stimulation: wide-dynamic-range (WDR) neurons (21%); nociceptive-specific (NS) neurons (67%); and inhibited (INH) neurons (13%). 2. No differences in the response properties or in the proportions of WDR, NS, and INH neurons were found in the CPu compared with the GP. Nociceptive neurons were located most often along the CPu-GP border. Additionally, neurons of similar functional classification were often clustered within 200-400 microns of each other along a single microelectrode track. 3. The receptive fields of nociceptive CPu and GP neurons were often large and bilateral; some receptive fields encompassed the entire body. The trigeminal region, especially the perioral area, was included in the receptive fields of nociceptive neurons more often (62 of 63 cells) than any other part of the body. However, no preference for any particular division of the trigeminal nerve was observed in the receptive fields. Some neurons had receptive fields that were discontinuous. 4. Noxious pinching of the skin significantly increased the spontaneous neuronal discharge of WDR and NS neurons by an average of 482 and 221%, respectively. There were no significant differences between the discharge adaptation rates of WDR and NS neurons. Afterdischarge activity was observed in some WDR and NS neurons. INH neurons decreased their resting activity levels by an average of 43% after a noxious pinch. 5. The von Frey stimulus threshold of WDR neurons (11.0 g/mm2) was significantly lower than that of NS neurons (33.6 g/mm2) and INH neurons (32.6 g/mm2). Mean stimulus thresholds of WDR, NS, and INH neurons determined by using calibrated forceps were 1.6, 4.8, and 2.2 g/mm2, respectively. 6. Individual stimulus-response functions of nociceptive neurons were best fit by a negatively accelerating (logarithmic) curves. However, WDR neurons had significantly steeper slopes than NS neurons. 7. The results demonstrate that a large proportion of somatosensory neurons within the neostriatum and globus pallidus (especially along the CPu-GP border) receive nociceptive information. These data are discussed in relation to several putative afferent nociceptive pathways projecting to the CPu and GP.(ABSTRACT TRUNCATED AT 400 WORDS)


1987 ◽  
Vol 57 (6) ◽  
pp. 1686-1704 ◽  
Author(s):  
K. C. Kajander ◽  
G. J. Giesler

The majority of neurons at the origin of the spinocervical tract are driven by noxious stimulation of their receptive fields. Surprisingly, previous studies have encountered only a small percentage of nociceptive neurons within the terminus of the spinocervical tract, the lateral cervical nucleus (LCN). To determine if previous reports have underestimated the proportion of nociceptive LCN neurons, 129 neurons within the nucleus were physiologically identified and examined in cats prepared using three different methods. Fifty-nine percent of the neurons studied in unanesthetized cats that were decerebrated and spinalized responded either differentially or exclusively to noxious mechanical stimulation of the skin within discrete receptive fields. LCN neurons also gave accelerating responses to increasingly more intense noxious thermal stimuli. LCN neurons are, therefore, capable of coding both the intensity and location of noxious stimuli. Only 6% of LCN neurons responded to noxious cutaneous stimuli in unanesthetized, decerebrated cats in which the spinal cord was intact. Only 4% of LCN neurons in intact urethan-anesthetized cats were driven by noxious stimulation. Several previous studies of the LCN have been performed in cats that were deeply anesthetized with barbiturates. Therefore, the effects of barbiturates on the nociceptive responses of LCN neurons were determined. Subanesthetic doses of intravenously administered barbiturates reduced or eliminated the responses of nociceptive LCN neurons to noxious thermal stimuli in decerebrated and spinalized cats. Responses to innocuous mechanical stimuli by these neurons were not blocked by barbiturates. Nociceptive LCN neurons in decerebrated and spinalized cats were somatotopically organized. Neurons with forelimb receptive fields were located in the ventromedial half of the LCN; neurons with hindlimb receptive fields were located in the dorsolateral half of the nucleus. This report and previous studies of the spinocervical tract suggest that the spinocervicothalamic pathway is capable of playing an important role in nociception.


1983 ◽  
Vol 49 (3) ◽  
pp. 674-685 ◽  
Author(s):  
L. Z. Wise ◽  
D. R. Irvine

1. The auditory responses of 207 single neurons in the intermediate and deep layers of the superior colliculus (SC) of barbiturate -or chloralose-anesthetized cats were recorded extracellularly. Sealed stimulating systems incorporating calibrated probe microphone assemblies were employed to present tone- and noise-burst stimuli. 2. All acoustically activated neurons responded with onset responses to noise bursts. Of those neurons also tested with tonal stimuli, approximately 30% were unresponsive over the frequency range tested (0.1-40 kHz), while the others had higher thresholds to tones than to noise. 3. Details of frequency responsiveness were obtained for 55 neurons; 21 were broadly tuned, while 34 were sharply tuned with clearly defined characteristic frequencies (CFs). All sharply tuned neurons had CFs greater than or equal to 10 kHz. 4. The majority of neurons (81%) responded with latencies in the range 8-20 ms; only 11% of neurons had latencies greater than 30 ms. 5. Binaural response properties were examined for 165 neurons. The great majority (79%) received monaural excitatory input only from the contralateral ear (EO). However, most EO cells were binaurally influenced, the contralateral response being either inhibited (EO/I; 96 of 131 units) or facilitated (EO/F; 33 of 131 units) by simultaneous ipsilateral stimulation. Small subgroups were monaurally excited by either ear (EE cells; 8%) or were unresponsive monaurally but responded strongly to binaural stimulation (OO/F cells; 7%). 6. EO/I, EO/F, and OO/F neurons showed characteristic forms of sensitivity to interaural intensity differences (IIDs). The IID functions of EO/I neurons would be expected to produce large contralateral spatial receptive fields with clearly defined medial borders, such as have been described in studies of deep SC neurons employing free-field stimuli. 7. Preliminary evidence suggests a possible topographic organization of IID sensitivity in deep SC, such that the steeply sloping portion of the function (corresponding to the medial edge of the receptive field) is shifted laterally for EO/I neurons located more caudally in the nucleus. 8. The auditory properties of deep SC neurons are compared with previous reports and implications for the organization of auditory input are considered. The binaural properties and auditory spatial fields of deep SC neurons suggest that any representation of auditory space in this structure is unlikely to be based on restricted spatial fields.


1990 ◽  
Vol 4 (4) ◽  
pp. 367-377 ◽  
Author(s):  
D. M. Guthrie ◽  
J. R. Banks

AbstractThe anatomy and physiology of the retinotectal pathway of the perch was investigated using physiological and histological techniques. Massed responses of the optic nerve to single shocks exhibited five distinct peaks. Single-unit responses to shocks indicate two groups of fast fibers correlating well with peaks I and II of the massed response. The flash-evoked response in nerve and tectum has three major phases (PSPI-III), with a marked low-threshold fast component. Patterns of flash-evoked response from single fibers vary, but the responses of fast transient fibers coincide with the timing of PSPI, and longer latency groups with PSPII-III. Units reflexly activated by efferents were also seen, and 12% of units were photically inexcitable.Surprisingly, few fibers responded well to a scanned spot light, unlike tectal cells, and receptive fields were often large (>70 deg). ON/OFF responses, evoked either by whole field or local illumination, were much commoner than pure ON or OFF responses.Effects of electrical stimulation or cautery of the tectum on the flash-evoked response of fiber bundles, via the efferents were marginal, but repetitive stimulation or section of the optic nerve produced clear-cut deficits in the slow components of the flash-evoked response of the nerve. Stimulation of the eighth nerve produced a complex long-latency, large-amplitude response in the optic nerve.The fiber spectrum of the optic nerve taken from electron micrographs revealed the presence of a relatively small group (less than 1%) of thick fibers with diameters between 3 μm and 10 μm that could be correlated with fast responses recorded from the optic nerve, and the remainder with axon diameters down to 0.2 μm providing the slow responses. The distribution of cell-body diameters from sectioned and wholemount material indicated a marked distinction between small and large ganglion cells. The total number of fibers in the nerve was estimated 868,840.


1989 ◽  
Vol 62 (6) ◽  
pp. 1270-1279 ◽  
Author(s):  
D. D. Price ◽  
J. G. McHaffie ◽  
M. A. Larson

1. Psychophysical experiments were initiated to determine the possible influence of increasing stimulus size on perceived pain intensity. Six trained human subjects (5 male, 1 female) made visual analogue scale (VAS) ratings for pain-sensation intensity and unpleasantness in response to nociceptive thermal stimuli. Test stimuli consisted of 5-s duration heat pulses (45-50 degrees C in 1 degrees increments) delivered by one, two, or three contact thermal probes (1 cm2 each) applied to the medial aspect of the anterior forearm. 2. The area of skin receiving noxious thermal stimuli was changed by randomly varying the number of thermodes activated. The effects of varying the distance between the thermal probes also were evaluated. In the first series of experiments, thermal-probe separation was kept close to 0; in subsequent experimental series, the thermodes were separated by either 5 or 10 cm. 3. In each experimental series, considerable spatial summation occurred in both pain-sensation intensity and unpleasantness dimensions of pain. This summation occurred throughout the nociceptive thermal range of 45-50 degrees C and was larger at suprathreshold temperatures (greater than or equal to 47 degrees C) than those near threshold (less than or equal to 46 degrees C). Unlike spatial summation of perceived warmth, that of pain was not characterized by systematic changes in power-function exponents but as approximately upward parallel displacements in double-logarithmic coordinates. 4. Thermal-probe separation over a range of 0-10 cm had no effects on spatial summation of pain-sensation intensity or pain unpleasantness. In contrast, increasing thermal-probe separation increased the subjects' ability to discriminate differences in stimulus size and their ability to detect correctly the number of thermal probes activated. 5. Because affective VAS ratings of unpleasantness were linearly related to, but distinctly and systematically less than, VAS ratings of pain-sensation intensity, it was clear that subjects responded quite differently to these two pain dimensions. Affective judgements were not additionally influenced by thermal probe separation and hence by the ability to perceive stimulus size or number of thermal probes activated. 6. The results indicate that powerful spatial-summation mechanisms exist for heat-induced pain. Spatial summation of pain is likely to be subserved both by local integration mechanisms at the level of single spinothalamic-tract neurons and by recruitment of central nociceptive neurons, because spatial summation of pain occurred to approximately equal extents under conditions of thermode separations over a distance of at least 20 cm.


1997 ◽  
Vol 77 (1) ◽  
pp. 299-308 ◽  
Author(s):  
Geoffrey M. Bove ◽  
Michael A. Moskowitz

Bove, Geoffrey M. and Michael A. Moskowitz. Primary Afferent Neurons Innervating Guinea Pig Dura. J. Neurophysiol. 77: 299–308, 1997. We made recordings from filaments of guinea pig nasociliary nerve to study response properties of afferent axons innervating the anterior superior sagittal sinus and surrounding dura mater. We analyzed 38 units in 14 experiments. Units were initially located with the use of mechanical stimuli, and were then characterized by their conduction velocity and sensitivities to mechanical, thermal, and chemical stimuli. Single-unit recordings revealed innervation of dura and superior sagittal sinus by slowly conducting axons, mostly in the unmyelinated range. The receptive fields were 1–30 mm2, and typically had one to three punctate spots of highest sensitivity. All units tested responded to topical application of chemical agents. Ninety-seven percent of units responded to 10−5 M capsaicin, 79% responded to a mixture of inflammatory mediators, and 37% responded to an acidic buffer (pH 5). These data underline the importance of chemical sensitivity in intracranial sensation. Heat and cold stimuli evoked responses in 56 and 41% of units tested, respectively. Although the response patterns during heating were typical of polymodal nociceptors innervating other tissues, the thresholds were lower than for other tissues (32.3–42°C). Cooling led to a phasic discharge, with thresholds between 25 and 32°C. Although units had different combinations of responses to mechanical, chemical, and thermal stimuli, when grouped by their sensitivities the groups did not differ regarding mechanical thresholds or presence of ongoing activity. This suggests that meningeal primary afferents are relatively homogeneous. Sensitivities of these units are in general consistent with nociceptors, although the thermal thresholds differ. These data provide the first detailed report of response properties of intracranial primary afferent units, likely to be involved in transmission of nociception and possibly mediation of intracranial pain.


2011 ◽  
Vol 106 (4) ◽  
pp. 1862-1874 ◽  
Author(s):  
Jan Churan ◽  
Daniel Guitton ◽  
Christopher C. Pack

Our perception of the positions of objects in our surroundings is surprisingly unaffected by movements of the eyes, head, and body. This suggests that the brain has a mechanism for maintaining perceptual stability, based either on the spatial relationships among visible objects or internal copies of its own motor commands. Strong evidence for the latter mechanism comes from the remapping of visual receptive fields that occurs around the time of a saccade. Remapping occurs when a single neuron responds to visual stimuli placed presaccadically in the spatial location that will be occupied by its receptive field after the completion of a saccade. Although evidence for remapping has been found in many brain areas, relatively little is known about how it interacts with sensory context. This interaction is important for understanding perceptual stability more generally, as the brain may rely on extraretinal signals or visual signals to different degrees in different contexts. Here, we have studied the interaction between visual stimulation and remapping by recording from single neurons in the superior colliculus of the macaque monkey, using several different visual stimulus conditions. We find that remapping responses are highly sensitive to low-level visual signals, with the overall luminance of the visual background exerting a particularly powerful influence. Specifically, although remapping was fairly common in complete darkness, such responses were usually decreased or abolished in the presence of modest background illumination. Thus the brain might make use of a strategy that emphasizes visual landmarks over extraretinal signals whenever the former are available.


2021 ◽  
Vol 118 (49) ◽  
pp. e2115772118
Author(s):  
Aneesha K. Suresh ◽  
Charles M. Greenspon ◽  
Qinpu He ◽  
Joshua M. Rosenow ◽  
Lee E. Miller ◽  
...  

Tactile nerve fibers fall into a few classes that can be readily distinguished based on their spatiotemporal response properties. Because nerve fibers reflect local skin deformations, they individually carry ambiguous signals about object features. In contrast, cortical neurons exhibit heterogeneous response properties that reflect computations applied to convergent input from multiple classes of afferents, which confer to them a selectivity for behaviorally relevant features of objects. The conventional view is that these complex response properties arise within the cortex itself, implying that sensory signals are not processed to any significant extent in the two intervening structures—the cuneate nucleus (CN) and the thalamus. To test this hypothesis, we recorded the responses evoked in the CN to a battery of stimuli that have been extensively used to characterize tactile coding in both the periphery and cortex, including skin indentations, vibrations, random dot patterns, and scanned edges. We found that CN responses are more similar to their cortical counterparts than they are to their inputs: CN neurons receive input from multiple classes of nerve fibers, they have spatially complex receptive fields, and they exhibit selectivity for object features. Contrary to consensus, then, the CN plays a key role in processing tactile information.


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