Receptive Fields and Response Properties of Neurons in the Star-Nosed Mole's Somatosensory Fovea

2002 ◽  
Vol 87 (5) ◽  
pp. 2602-2611 ◽  
Author(s):  
Robert N. S. Sachdev ◽  
Kenneth C. Catania

Star-nosed moles have an extraordinary mechanosensory system consisting of 22 densely innervated nasal appendages covered with thousands of sensitive touch domes. A single appendage acts as the fovea and the star is constantly shifted to touch this foveal appendage to objects of interest. Here we investigated the receptive fields on the star and the response properties of 144 neurons in the mole's primary somatosensory cortex (S1). Excitatory receptive fields were defined by recording multiunit activity from the S1 representations of the nasal appendages that form the star, while stimulating the touch domes on the skin surface with a small probe. Receptive fields were among the smallest reported for mammalian glabrous skin, averaging <1 mm2. The smallest receptive fields were found for the fovea representation, corresponding to its greater cortical magnification. Single units were then isolated, primarily from the representation of the somatosensory fovea, and the skin surface was stimulated with a small probe attached to a piezoelectric wafer controlled by a computer interface. The response properties of neurons and the locations of inhibitory surrounds were evaluated with two complementary approaches. In the first set of experiments, single microelectrodes were used to isolate unit activity in S1, and data were collected for stimulation to different areas of the sensory star. In the second set of experiments, a multi-electrode array (4 electrodes spaced at 200 μm in a linear sequence) was used to simultaneously record from isolated units in different cortical areas representing different parts of the sensory periphery. These experiments revealed a short-latency excitatory discharge to stimulation of the fovea followed by a long-lasting suppression of spontaneous activity. Sixty-one percent of neurons responded with an excitatory off response at the end of the stimulus; the remaining 39% of cells did not respond or were inhibited at stimulus offset. Stimulation of areas surrounding the central receptive field often revealed inhibitory surrounds. Forty percent of the neurons that responded to mechanosensory stimulation of the receptive field center were inhibited by stimulation of surrounding areas of skin on the same appendage. In contrast to neurons in rodent barrels, few neurons within a stripe representing an appendage responded to stimulation of neighboring (nonprimary) appendages on the snout. The small receptive fields, short latencies, and inhibitory surrounds are consistent with the star's role in rapidly determining the locations and identities of objects in a complex tactile environment.


1996 ◽  
Vol 75 (6) ◽  
pp. 2441-2450 ◽  
Author(s):  
D. D. Rasmusson

1. Single neurons in the ventroposterior lateral thalamic nucleus were studied in 10 anesthetized raccoons, 4 of which had undergone amputation of the fourth digit 4-5 mo before recording. Neurons with receptive fields on the glabrous skin of a forepaw digit were examined in response to electrical stimulation of the “on-focus” digit that contained the neuron's receptive field and stimulation of an adjacent, “off-focus” digit. 2. In normal raccoons all neurons responded to on-focus stimulation with an excitation at a short latency (mean 13 ms), whereas only 63% of the neurons responded to off-focus digit stimulation. The off-focus responses had a longer latency (mean 27.2 ms) and a higher threshold than the on-focus responses (800 and 452 microA, respectively). Only 3 of 32 neurons tested with off-focus stimulation had both a latency and a threshold within the range of on-focus values. Inhibition following the excitation was seen in the majority of neurons with both types of stimulation. 3. In the raccoons with digit removal, the region of the thalamus that had lost its major peripheral input (the “deafferented” region) was distinguished from the normal third and fifth digit regions on the basis of the sequence of neuronal receptive fields within a penetration and receptive field size as described previously. 4. Almost all of the neurons in the deafferented region (91%) were excited by stimulation of one or both adjacent digits. The average latency for these responses was shorter (15.3 ms) and the threshold was lower than was the case with off-focus stimulation in control animals. These values were not significantly different from the responses to on-focus stimulation in the animals with digit amputation. 5. These results confirm that reorganization of sensory pathways can be observed at the thalamic level. In addition to the changes in the somatotopic map that have been shown previously with the use of mechanical stimuli, the present paper demonstrates an improvement in several quantitative measures of single-unit responses. Many of these changes suggest that this reorganization could be explained by an increased effectiveness of preexisting, weak connections from the off-focus digits; however, the increase in the proportion of neurons responding to stimulation of adjacent digits may indicate that sprouting of new connections also occurs.



1990 ◽  
Vol 2 (1) ◽  
pp. 71-84 ◽  
Author(s):  
Kamil A. Grajski ◽  
Michael M. Merzenich

The inverse magnification rule in cortical somatotopy is the experimentally derived inverse relationship between cortical magnification (area of somatotopic map representing a unit area of skin surface) and receptive field size (area of restricted skin surface driving a cortical neuron). We show by computer simulation of a simple, multilayer model that Hebb-type synaptic modification subject to competitive constraints is sufficient to account for the inverse magnification rule.



1990 ◽  
Vol 64 (4) ◽  
pp. 1134-1148 ◽  
Author(s):  
S. N. Currie ◽  
P. S. Stein

1. We demonstrated multisecond increases in the excitability of the rostral-scratch reflex in the turtle by electrically stimulating the shell at sites within the rostral-scratch receptive field. To examine the cellular mechanisms for these multisecond increases in scratch excitability, we recorded from single cutaneous afferents and sensory interneurons that responded to stimulation of the shell within the rostral-scratch receptive field. A single segment of the midbody spinal cord (D4, the 4th postcervical segment) was isolated in situ by transecting the spinal cord at the segment's anterior and posterior borders. The isolated segment was left attached to its peripheral nerve that innervates part of the rostral-scratch receptive field. A microsuction electrode (4-5 microns ID) was used to record extracellularly from the descending axons of cutaneous afferents and interneurons in the spinal white matter at the posterior end of the D4 segment. 2. The turtle shell is innervated by slowly and rapidly adapting cutaneous afferents. All cutaneous afferents responded to a single electrical stimulus to the shell with a single action potential. Maintained mechanical stimulation applied to the receptive field of some slowly adapting afferents produced several seconds of afterdischarge at stimulus offset. We refer to the cutaneous afferent afterdischarge caused by mechanical stimulation of the shell as "peripheral afterdischarge." 3. Within the D4 spinal segment there were some interneurons that responded to a brief mechanical stimulus within their receptive fields on the shell with short afterdischarge and others that responded with long afterdischarge. Short-afterdischarge interneurons responded to a single electrical pulse to a site in their receptive fields either with a brief train of action potentials or with a single action potential. Long-afterdischarge interneurons responded to a single electrical shell stimulus with up to 30 s of afterdischarge. Long-afterdischarge interneurons also exhibited strong temporal summation in response to a pair of electrical shell stimuli delivered up to several seconds apart. Because all cutaneous afferents responded to an electrical shell stimulus with a single action potential, we conclude that electrically evoked afterdischarge in interneurons was produced by neural mechanisms in the spinal cord; we refer to this type of afterdischarge as "central afterdischarge." 4. These results demonstrate that neural mechanisms for long-lasting excitability changes in response to cutaneous stimulation reside in a single segment of the spinal cord. Cutaneous interneurons with long afterdischarge may serve as cellular loci for multise



1979 ◽  
Vol 42 (4) ◽  
pp. 954-974 ◽  
Author(s):  
S. C. Rosen ◽  
K. R. Weiss ◽  
I. Kupfermann

1. The cells of two clusters of small neurons on the ventrocaudal surface of each hemicerebral ganglion of Aplysia were found to exhibit action potentials following tactile stimuli applied to the skin of the head. These neurons appear to be mechanosensory afferents since they possess axons in the nerves innervating the skin and tactile stimulation evokes spikes with no prepotentials, even when the cell bodies are sufficiently hyperpolarized to block some spikes. The mechanosensory afferents may be primary afferents since the sensory response persists after chemical synaptic transmission is blocked by bathing the ganglion and peripheral structures in seawater with a high-Mg2+ and low-Ca2+ content. 2. The mechanosensory afferents are normally silent and are insensitive to photic, thermal, and chemical stimuli. A punctate tactile stimulus applied to a circumscribed region of skin can evoke a burst of spikes. If the stimulus is maintained at a constant forces, the mechanosensory response slowly adapts over a period of seconds. Repeated brief stimuli have little or no effect on spike frequency within a burst. 3. Approximately 81% of the mechanoafferent neurons have a single ipsilateral receptive field. The fields are located on the lips, the anterior tentacles, the dorsal portion of the head, the neck, or the perioral zone. Because many cells have collateral axons in the cerebral connectives, receptive fields elsewhere on the body are a possibility. The highest receptive-field density was associated with the lips. Within each area, receptive fields vary in size and shape. Adjacent fields overlap and larger fields frequently encompass several smaller ones. The features of some fields appear invariant from one animal to the next. A loose form of topographic organization of the mechanoafferent cells was observed. For example, cells located in the medial cluster have lip receptive fields, and most cells in the posterolateral portion of the lateral clusters have tentacle receptive fields. 4. Intracellular stimulation of individual mechanoafferents evokes short and constant-latency EPSPs in putative motor neurons comprising the identified B-cell clusters of the cerebral ganglion. On the basis of several criteria, these EPSPs appear to be several criteria, these EPSPs appear to be chemically mediated and are monosynaptic. 5. Repetitive intracellular stimulation of individual mechanoafferent neurons at low rates results in a gradual decrement in the amplitude of the EPSPs evoked in B cluster neurons. EPSP amplitude can be restored following brief periods of rest, but subsequent stimulation leads to further diminution of the response. 6. A decremented response cannot be restored by strong mechanical stimulation outside the receptive field of the mechanoafferent or by electrical stimulation of the cerebral nerves or connectives...



1978 ◽  
Vol 41 (6) ◽  
pp. 1511-1534 ◽  
Author(s):  
A. D. Craig ◽  
D. N. Tapper

1. The lateral cervical nucleus (LCN) was investigated with extracellular recordings in the anesthetized cat. A total of 556 LCN units were characterized; the locations of most of these were histologically verified. Half of these had receptive fields on the rostral third of the ipsilateral body surface including the face; 14% had fields on the thorax or abdomen, 33% had fields on the hindlimb or tail, and about 3% had receptive fields larger than one limb. 2. The LCN was observed to be somatotopically organized in experiments using angled microelectrode penetrations. Hindlimb units were dorsolateral, forelimb units ventromedial, and face units most medial within the LCN. In regions where LCN cells were present only in the medial portion of the dorsolateral funiculus, they were all forelimb units. 3. A special subpopulation (17%) of cells were clustered most ventromedially in the LCN. These units had large or disjoint receptive fields, and/or responded to deep, visceral, or noxious stimulation. A third of these did not project in the medial lemniscus (ML); many were synaptically activated by stimulation of the ML. Those that did project in the ML had significantly longer latencies than all other LCN units. It is suggested that this subpopulation contains local LCN interneurons. 4. The specific mechanoreceptor inputs were identified for each of 121 projecting LCN units. Receptor inputs were uniform across each receptive field; that is, each unit that responded to a given receptor type was observed to respond to receptors of that type throughout its receptive field. Input from large-fiber-diameter, velocity-sensitive mechanoreceptors was predominant. The absence of input from slowly adapting type I and II receptors and from joint receptors was confirmed. A significant number of units (17.3%) could be driven by only one receptor type. The LCN sample profile agrees closely with the receptor representation in the hindlimb portion of the spinocervical tract. It is concluded that these data that anatomic specification of convergence occurs in the LCN with respect to receptor connectivity, and that this specification originates in lamina IV of the dorsal horn. 5. Stimulation of the dorsal column nuclei synaptically excited 23% of the LCN units tested. In two cases it was possible to demonstrate, by collision, that this occurred via collaterals of spinocervical tract axons. It is concluded that some spinocervical axons have collaterals terminating in the rostral parts of the dorsal column nuclei.



1994 ◽  
Vol 72 (3) ◽  
pp. 1080-1102 ◽  
Author(s):  
T. J. Park ◽  
G. D. Pollak

1. In this study we examine the effects of GABAergic inhibition on the response properties and the constructed azimuthal receptive fields of 54 excitatory/inhibitory (EI) neurons tuned to 60 kHz in the inferior colliculus of the mustache bat. The constructed azimuthal receptive fields predict the spike counts that would be evoked by different intensities of 60-kHz sounds presented from each of 13 azimuthal locations in the frontal sound field. 2. Action potentials were recorded with a micropipette attached to a multibarrel glass electrode. Bicuculline, an antagonist specific for gamma-aminobutyric acid-A (GABAA) receptors, was iontophoretically applied through the multibarrel electrode. Both monaural and binaural response properties were initially recorded at a variety of interaural intensity disparities (IIDs) and absolute intensities, and the same response properties were subsequently assessed while GABAergic inhibition was blocked by bicuculline. Azimuthal receptive fields both before and during the application of bicuculline were constructed from response properties obtained with earphones after correcting for the directional properties of the ear and the IIDs generated by 60-kHz sounds presented from a variety of azimuthal locations. 3. Bicuculline had virtually no effect on either the monaural or binaural properties of 19 cells (35%). The constructed azimuthal receptive fields of these cells were also unaffected by bicuculline. Presumably the properties of these cells were formed in a lower nucleus, most likely the contralateral lateral superior olive (LSO), and were imposed on the collicular cell via the crossed projection from the LSO to the inferior colliculus, which is known to be excitatory. 4. In more than half of the neurons (65%) GABAergic inhibition influenced one or more features of the cell's response properties and thus its azimuthal receptive field. Some response properties were formed in the colliculus through GABAergic inhibition, whereas others appear to have been shaped initially in a lower nucleus and then further modified by GABAergic inhibition in the inferior colliculus. Moreover, a number of features of GABAergic inhibition that acted on inferior collicular cells were evoked by stimulation of the contralateral (excitatory) ear, whereas other features were influenced by stimulation of the ipsilateral (inhibitory) ear. 5. In 20 cells (37%) blocking GABAergic inhibition reduced or abolished the inhibition evoked by the ipsilateral ear. The receptive fields of cells in which the ipsilaterally evoked inhibition was reduced by bicuculline expanded further into the ipsilateral sound field than they did before bicuculline.(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)



1988 ◽  
Vol 1 (4) ◽  
pp. 377-385 ◽  
Author(s):  
Michael W. Levine ◽  
Roger P. Zimmerman

AbstractA new form of receptive field map, the response-component map, was developed to identify points within a receptive field that produce similar response patterns. The fields were probed with discretely flashed small spots of light. The magnitudes of the responses to stimulus onset and to stimulus offset elicited at each point were represented on the map by a vector radiating from the position representing the location of that point. Thus, response-component maps preserve the spatial distributions of responsivity and temporal nonlinearities. Points with similar response patterns were identified from a scatterplot in which the response at each spatial position was located in a plane representing the angles of the response-component vectors. Points with similar response characteristics that were also spatially contiguous were considered as a distinct response subregion within the receptive field.Barely 10% of the receptive fields of goldfish ganglion cells mapped with this technique proved as simple as the traditional concentric field described for retinal cells. In at least 17% of the cases, the field showed three concentric rings, with a very small “inner center” within the center of the field. In at least 50% of the cases, response subregions of different type lay side by side, rather than in a concentric configuration. Some subregions could be differentiated by the relative strengths of the responses to onset and offset of the stimulus spot, supporting the hypothesis that a push-pull system generates ganglion cell responses. Subregions were evident in successive mappings of the same cell, demonstrating they are not due to the vagaries of individual responses. They probably represent the spatial domains (or their intersections) of individual interneurons distal to the retinal ganglion cells. It is possible that position within the receptive field may be coded by the temporal pattern of the responses.



2001 ◽  
Vol 85 (5) ◽  
pp. 2111-2129 ◽  
Author(s):  
Jonathan B. Levitt ◽  
Robert A. Schumer ◽  
S. Murray Sherman ◽  
Peter D. Spear ◽  
J. Anthony Movshon

It is now well appreciated that parallel retino-geniculo-cortical pathways exist in the monkey as in the cat, the species in which parallel visual pathways were first and most thoroughly documented. What remains unclear is precisely how many separate pathways pass through the parvo- and magnocellular divisions of the macaque lateral geniculate nucleus (LGN), what relationships—homologous or otherwise—these pathways have to the cat's X, Y, and W pathways, and whether these are affected by visual deprivation. To address these issues of classification and trans-species comparison, we used achromatic stimuli to obtain an extensive set of quantitative measurements of receptive field properties in the parvo- and magnocellular laminae of the LGN of nine macaque monkeys: four normally reared and five monocularly deprived of vision by lid suture near the time of birth. In agreement with previous studies, we find that on average magnocellular neurons differ from parvocellular neurons by having shorter response latencies to optic chiasm stimulation, greater sensitivity to luminance contrast, and better temporal resolution. Magnocellular laminae are also distinguished by containing neurons that summate luminance over their receptive fields nonlinearly (Y cells) and whose temporal response phases decrease with increasing stimulus contrast (indicative of a contrast gain control mechanism). We found little evidence for major differences between magno- and parvocellular neurons on the basis of most spatial parameters except that at any eccentricity, the neurons with the smallest receptive field centers tended to be parvocellular. All parameters were distributed unimodally and continuously through the parvo- and magnocellular populations, giving no indications of subpopulations within each division. Monocular deprivation led to clear anatomical effects: cells in deprived-eye laminae were pale and shrunken compared with those in nondeprived eye laminae, and Cat-301 immunoreactivity in deprived laminae was essentially uniformly abolished. However, deprivation had only subtle effects on the response properties of LGN neurons. Neurons driven by the deprived eye in both magno- and parvocellular laminae had lower nonlinearity indices (i.e., summed signals across their receptive fields more linearly) and were somewhat less responsive. In magnocellular laminae driven by the deprived eye, neuronal response latencies to stimulation of the optic chiasm were slightly shorter than those in the nondeprived laminae, and receptive field surrounds were a bit stronger. No other response parameters were affected by deprivation, and there was no evidence for loss of a specific cell class as in the cat.



1980 ◽  
Vol 43 (6) ◽  
pp. 1673-1699 ◽  
Author(s):  
V. Golovchinsky

1. The responses of single cuneate neurons to controled mechanical stimulation of skin were recorded in cats lightly anesthetized with a nitrous oxide-halothane mixture. The discharge patterns and peripheral receptive-field characteristics were studied in neurons driven by sensitive cutaneous mechanoreceptors, including slowly adapting skin mechanoreceptors. Virtually all cuneate neurons display maximum discharge during the velocity component of displacement. 2. Among cuneate neurons encountered in this study, approximately 46% were driven by guard hair mechanoreceptors, 15% were driven by field receptors, and 13% were driven by slowly adapting skin receptors. Neurons responding to stimulation of deep tissues (including claws) were not studied with controlled mechanical stimulation and accounted for 19%. The rest of the neurons were driven by Pacinian corpuscles, received afferent inputs from several different first-order afferents, or were not definitely identified. There was no clear evidence of down hair or high-threshold mechanoreceptor representation. 3. The discharge pattern in response to a constant-velocity stimulus proved most valuable in describing submodality classes of neurons driven by hair and field receptors since sensitivity of these neurons to dynamic and to static phases of stimulation constitute respective continua and, thus, preclude sharp separation into distinct groups. 4. The majority of neurons displayed response properties and receptive fields similar to those of first-order afferents. A minority of cells had receptive fields that were larger than those of primary afferents, with nearly identical modality and velocity characteristics throughout the receptive field. 5. Approximately 2% of recorded neurons displayed convergent properties not encountered in first-order afferents, including neurons driven from receptors of different modalities or from discontinuous receptive fields. 6. Inhibition of neuronal firing generated from outside the receptive field was rarely seen, possibly due to anesthetic conditions. In a small number of neurons, irregularities in the discharge were observed that might indicate inhibitory influences originating from within the receptive field.



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