Azimuthal receptive fields are shaped by GABAergic inhibition in the inferior colliculus of the mustache bat

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)

1994 ◽  
Vol 71 (6) ◽  
pp. 1999-2013 ◽  
Author(s):  
L. Yang ◽  
G. D. Pollak

1. We studied the monaural and binaural response properties of 99 neurons in the dorsal nucleus of the lateral lemniscus (DNLL) of the mustache bat before and during the iontophoretic application of antagonists that blocked gamma-aminobutyric acid-A (GABAA) receptors (bicuculline) or glycine receptors (strychnine). All cells were driven by monaural stimulation of the contralateral ear, whereas monaural stimulation of the ipsilateral ear never evoked discharges. The binaural properties of 81 neurons were determined by holding the intensity constant at the contralateral ear and presenting a variety of intensities to the ipsilateral ear. This procedure generated interaural intensity disparity (IID) functions and allowed us to determine the effect of ipsilaterally evoked inhibition on a constant excitatory drive evoked by the contralateral ear. 2. One of the main findings is that the IID functions in the majority of DNLL neurons were not affected by application of either strychnine or bicuculline. Blocking glycinergic inhibition with strychnine had no effect on the IID functions in 75% of the cells studied. However, strychnine did change the IID functions in approximately 25% of the DNLL population. In those cells glycinergic inhibition appeared to be partially, or, in a few cases, entirely responsible for the ipsilaterally evoked spike suppression. In contrast, blocking GABAergic inhibition with bicuculline had no discernible effect on the ipsilaterally evoked spike suppression in any of the excitatory/inhibitory cells that we recorded. GABAergic inhibition, therefore, plays no role in the formation of IID functions of neurons in the DNLL. Furthermore, the results suggest that glycinergic inhibition also does not contribute to the suppression of spikes evoked by stimulation of the contralateral ear in the vast majority of DNLL neurons. 3. Although the majority of IID functions were not influenced when either GABAergic or glycinergic innervation was blocked, ipsilateral stimulation alone evoked both a glycinergic and GABAergic inhibition in most DNLL cells. These inhibitory events were demonstrated in 18 other cells by evoking discharges with the iontophoretic application of glutamate. Stimulating the ipsilateral ear alone under these conditions caused a suppression of the glutamate-evoked discharges. Furthermore, the spike suppression persisted for a period of time that was longer than the duration of the tone burst at the ipsilateral ear. 4. The application of bicuculline or strychnine had different effects on the glutamate-elicited spikes. Bicuculline reduced the duration of the inhibition, and it was always the latter portion of the inhibition that was abolished by bicuculline. In more than half of the cells studied strychnine also reduced the duration of the inhibition.(ABSTRACT TRUNCATED AT 400 WORDS)


1992 ◽  
Vol 68 (2) ◽  
pp. 605-619 ◽  
Author(s):  
H. A. Swadlow

1. Extracellular action potentials were recorded from antidromically activated efferent neurons in visual, somatosensory, and motor cortex of the awake rabbit using low-impedance metal microelectrodes. Efferent neurons were also activated by current pulses delivered near the soma [juxtasomal current pulses (JSCPs)] through the recording microelectrode. Action potentials generated by JSCPs were not directly observed (because of the stimulus artifact), but were inferred with the use of a collision paradigm. Efferent populations studied include callosal neurons [CC (n = 80)], ipsilateral corticocortical neurons [C-IC (n = 21)], corticothalamic neurons of layer 6 [CF-6 (n = 57)], and descending corticofugal neurons of layer 5 [CF-5, corticotectal neurons of the visual cortex (n = 48)]. 2. Most CC neurons (45/46) and all C-IC (8/8) and CF-6 neurons (39/39) were directly activated by JSCPs at near-threshold intensities. Some CF-5 neurons (9/38), however, showed evidence of indirect activation. All efferent classes had similar current thresholds (means 1.85-2.10 microA) to direct activation by JSCPs, and thresholds were inversely related to extracellular spike amplitude. For each neuron, the range of JSCP intensities that generated response probabilities of between 0.2 and 0.8 was measured, and this "range of uncertainty" was significantly greater in CF-5 neurons (mean 32.7% of threshold) than in CC (mean 19.0%) or CF-6 (mean 20.4%) neurons. 3. Several factors indicate that the threshold of efferent neurons to JSCPs is very sensitive to excitatory and inhibitory synaptic inputs. Iontophoretic applications of gamma-aminobutyric acid (GABA) increased the threshold to JSCPs, and glutamate reduced the threshold. Electrical stimulation of afferent pathways at intensities just below threshold for eliciting action potentials resulted in a dramatic decrease in JSCP threshold. This initial short-latency threshold decrease was specific to stimulation of particular afferent pathways and is thought to reflect excitability changes associated with EPSPs. Examination of such subliminal responses revealed subthreshold synaptic inputs that were not revealed by examination of all-or-none action potentials. In contrast to the specificity of the short-latency threshold decrease, a long-lasting increase in JSCP threshold was seen in virtually all neurons after stimulation of each of the afferent pathways tested. This increase in threshold usually began 20-40 ms after stimulation, lasted for 100-200 ms, and is thought to reflect excitability changes associated with a long-lasting inhibitory postsynaptic potential (IPSP) seen in many cortical neurons. 4. Many neurons in primary somatosensory cortex of rat, cat, and rabbit have no demonstrable receptive fields.(ABSTRACT TRUNCATED AT 400 WORDS)


1995 ◽  
Vol 74 (4) ◽  
pp. 1701-1713 ◽  
Author(s):  
A. Klug ◽  
T. J. Park ◽  
G. D. Pollak

1. The mammalian inferior colliculus contains large populations of binaural cells that are excited by stimulation of the contralateral ear and are inhibited by stimulation of the ipsilateral ear, and are called excitatory/inhibitory (EI) cells. Neurons with EI properties are initially created in the lateral superior olive (LSO), which, in turn, sends strong bilateral projections to the inferior colliculus. The questions that we address in this report are 1) whether the inhibition evoked by stimulation of the ipsilateral ear occurs at the inferior colliculus or whether it occurs in a lower nucleus, presumably the LSO; and 2) if the ipsilaterally evoked inhibition occurs at the inferior colliculus, is the inhibition a consequence of glycinergic innervation or is it a consequence of GABAergic innervation. To study these questions, we recorded from 61 EI neurons in the inferior colliculus of the mustache bat before and during the iontophoretic application of the glycine receptor antagonist, strychnine. We also tested the effects of the gamma-aminobutyric acid-A (GABAA) receptor antagonist, bicuculline, on 38 of the 61 neurons that were tested with strychnine. The main finding is that glycinergic or GABAergic inhibition, or both, contribute to the ipsilaterally evoked inhibition in approximately 50% of the EI neurons in the inferior colliculus. 2. Strychnine and bicuculline had different effects on the magnitude of the spike counts evoked by stimulation of the contralateral (excitatory) ear. On average, strychnine caused the maximum spike count evoked by contralateral stimulation to increase by only 23%. The relatively small effects of strychnine on response magnitude are in marked contrast to the effects of bicuculline, which usually caused much larger increases in spike counts. For example, although strychnine caused spike counts to more than double in approximately 25% of the collicular neurons, bicuculline caused a doubling of the spike count in approximately 60% of the cells. 3. The inhibitory influences of ipsilateral stimulation were evaluated by driving the neurons with a fixed intensity at the contralateral ear and then documenting the reductions in spike counts due to the presentation of progressively higher intensities at the ipsilateral ear. In 64% of the neurons sampled, blocking glycinergic inhibition with strychnine had little or no effect on the ipsilaterally evoked inhibition. These cells remained as strongly inhibited during the application of strychnine as they did before its application. In addition, the ipsilateral intensity that produced complete or nearly complete spike suppression in the predrug condition was also unchanged by strychnine. 4. In 36% of the neurons, strychnine markedly reduced the degree of ipsilaterally evoked spike suppression. In five of these neurons, there was a complete elimination of the ipsilateral inhibition: these neurons were transformed from strongly inhibited EI neurons into monaural neurons. 5. The influence of both strychnine and bicuculline was tested sequentially in 38 neurons. In about one-half of these cells, (53%, 20/38) the ipsilaterally evoked inhibition was unaffected by either drug. In 10 other units (26%), both drugs substantially reduced or eliminated the ipsilaterally evoked inhibition. In most of these cells, both bicuculline and strychnine reduced the ipsilaterally evoked inhibition to a similar degree. In the remaining eight cells studied with both drugs (21%), the ipsilaterally evoked inhibition was reduced or eliminated by one of the drugs, but not by both. 6. These results show that both glycinergic and GABAergic projections influence the ipsilaterally evoked inhibition in about one-half of the EI neurons in the inferior colliculus. The glycinergic inhibition elicited by ipsilateral stimulation is most likely due to projections from the ipsilateral lateral superior olive, whereas the GABAergic inhibition evoked by ipsilateral stimulation is most likely caused b


1978 ◽  
Vol 41 (4) ◽  
pp. 837-847 ◽  
Author(s):  
L. M. Aitkin ◽  
H. Dickhaus ◽  
W. Schult ◽  
M. Zimmermann

1. The discharges of 129 units were studied in the external nucleus of the inferior colliculus of 11 anesthetised and paralyzed cats. This region is known to receive fibers from auditory nuclei and the dorsal column nuclei. 2. Stimuli used were pure tone bursts, monaural or binaural, tactile stimulation of the body surface, and electrical stimulation of the dorsal columns (DC) at a low cervical level and of the contralateral and ipsilateral tibial nerves. 3. Forty-six percent of units were only influenced by one type of stimulation (26% auditory, 20% DC). Of the remaining bimodally influenced units, the majority was excited by pure tone stimuli and inhibited by DC stimulation. 4. A small proportion of the total population (18%) was excited by both DC and auditory input, and units sensitive to both tones and tactile stimulation of the skin were rare (4%). 5. Auditory tuning curves were generally very broad compared with those of units in the central nucleus of the inferior colliculus. Similarly, somatic receptive fields were large and usually extended over a whole limb. 6. The majority of tone-responsive units were influenced binaurally (70%); most somatic receptive fields were located on the contralateral fore- or hindlimb (16/18). 7. The results indicate that both auditory and somatosensory information is contained in the discharges of units in the external nucleus of the inferior colliculus. 8. Speculations are made about the role of this nucleus in descending auditory input to the spinal cord and in the comparison of auditory and cutaneous information during sound-evoked coordinated body movements.


1997 ◽  
Vol 77 (5) ◽  
pp. 2723-2735 ◽  
Author(s):  
Richard D. Lane ◽  
Herbert P. Killackey ◽  
Robert W. Rhoades

Lane, Richard D., Herbert P. Killackey, and Robert W. Rhoades. Blockade of GABAergic inhibition reveals reordered cortical somatotopic maps in rats that sustained neonatal forelimb removal. J. Neurophysiol. 77: 2723–2735, 1997. A previous study from this laboratory demonstrated that forelimb removal at birth results in invasion of the cuneate nucleus (CN) by sciatic nerve axons and the development of CN cells including thalamic projection neurons with receptive fields that include both the forelimb stump and the hindlimb. However, recordings from unit clusters in lamina IV of the primary somatosensory cortex (SI) of these animals revealed the presence of only a very few sites in the forelimb stump representation where responses to hindlimb stimulation could also be recorded. In the present study we tested the possibility that input from the hindlimb was suppressed in lamina IV of the cortical stump representation via GABAergic inhibitory mechanisms by mapping this cortical region, applying the γ-aminobutyric acid-A (GABAA) and GABAB receptor antagonists bicuculline and phaclofen (50 μM each), and then remapping the same sites. In six neonatally manipulated rats, 15 of 242 sites (6.2%) in the stump representation responded to hindlimb stimulation before GABA receptor blockade and 107 (44.2%) of the same sites responded to stimulation of the hindlimb during blockade ( P < 0.05). In six normal adult rats, 7 of 264 sites (2.7%) in the forelimb representation responded to hindlimb stimulation before the application of bicuculline and phaclofen. During GABA receptor blockage, 31 of these sites (11.7%) responded to such stimulation ( P < 0.02 vs. the untreated normal cortex and P < 0.01 vs. the neonatally manipulated rats treated with GABA blockers). To specifically test the role of GABAA versus GABAB receptors in the inhibition of hindlimb input to the SI stump representation in rats that sustained neonatal forelimb removal, either bicuculline or phaclofen alone was applied to SI in nine neonatally manipulated animals. In four rats treated with bicuculline, 12 of 184 sites (6.5%) in the stump representation responded to hindlimb stimulation before treatment and 61 of 184 sites (33.2%) responded to such stimulation during application ( P < 0.01). In animals ( n = 5) treated with phaclofen, 18 of 251 sites (7.2%) responded to hindlimb stimulation before treatment and 64 of these sites (25.5%) responded to such stimulation during application ( P < 0.05). There was no significant difference between the results obtained with bicuculline alone, phaclofen alone, or the two GABA blockers delivered together ( P > 0.05). These results indicate that hindlimb input to the portion of SI representing the forelimb stump is functionally suppressed in rats that have sustained neonatal forelimb removal and that GABAergic inhibition, mediated by both GABAA and GABAB receptors, is involved in this process.


1997 ◽  
Vol 78 (2) ◽  
pp. 767-779 ◽  
Author(s):  
David McAlpine ◽  
Russell L. Martin ◽  
Jennifer E. Mossop ◽  
David R. Moore

McAlpine, David, Russell L. Martin, Jennifer E. Mossop, and David R. Moore. Response properties of neurons in the inferior colliculus of the monaurally deafened ferret to acoustic stimulation of the intact ear. J. Neurophysiol. 78: 767–779, 1997. Response properties of neurons in the central nucleus of the inferior colliculus (ICC) were investigated after unilateral cochlear removal at various ages during infancy. Nineteen ferrets had the right cochlea surgically ablated, either in adulthood or on postnatal day (P) 5, 25, or 40, 3–18 mo before recording. Adult ablations were made on the same day as (“acute,” n = 3), or 2–3 mo before (“chronic,” n = 3), recording. Two ferrets were left binaurally intact. Single-unit ( n = 702) and multiunit ( n = 1,819) recordings were made in the ICC of barbiturate-anesthetized ferrets ipsilateral (all ages) or contralateral (P5 and acute adult only) to the intact ear. In binaurally intact animals, tonal stimulation of the contralateral ear evoked excitatory activity at the majority (94%) of recording loci, whereas stimulation of the ipsilateral ear evoked activity at only 33% of recording loci. In acutely ablated animals, the majority of contralateral (90%) and ipsilateral (70%) loci were excited by tonal stimulation of the intact ear. In chronically ablated animals, 80–90% of loci were excited by ipsilateral stimulation. Single-unit thresholds were generally higher for low-best frequency (BF) than for high-BF units, and higher in the ipsilateral than in the contralateral ICC. Analysis of covariance showed highly significant differences between all of the ipsilateral and contralateral groups, but no effects of age at ablation or survival time following ablation, other than that the group ablated at P25 had higher mean ipsilateral thresholds than the groups ablated at P5 or, acutely, in adulthood. Cochlear ablation at P5, 25, or 40 resulted in a significant increase in dynamic ranges of ipsilateral ICC unit rate-intensity functions relative to acutely ablated animals. Dynamic ranges of units in the contralateral ICC of P5-ablated ferrets were also significantly increased compared with those of acutely ablated animals. Cochlear ablation at P5, 25, or 40 resulted in a significant increase in single-unit spontaneous discharge rates in the ICC ipsilateral but not contralateral (P5 only) to the intact ear. These data show that unilateral cochlear removal in adult ferrets leads to a rapid and dramatic increase in the proportion of neurons in the ICC ipsilateral to the intact ear that is excited by acoustic stimulation of that ear. In addition, the data confirm that, in ferrets, cochlear removal in infancy leads to a further increase in responsiveness of individual neurons in the ipsilateral ICC. Finally, the data show that responses in the ICC contralateral to the intact ear are largely but not completely unchanged by unilateral cochlear removal.


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.


2012 ◽  
Vol 91 (4) ◽  
pp. 401-406 ◽  
Author(s):  
D.K. Ahn ◽  
E.A. Doutova ◽  
K. McNaughton ◽  
A.R. Light ◽  
M. Närhi ◽  
...  

The response properties of tooth pulp neurons that respond to noxious thermal stimulation of the dental pulp have been not well-studied. The present study was designed to characterize the response properties of tooth pulp neurons to noxious thermal stimulation of the dental pulp. Experiments were conducted on 25 male ferrets, and heat stimulation was applied by a computer-controlled thermode. Only 15% of tooth pulp neurons (n = 39) responded to noxious thermal stimulation of the teeth. Tooth pulp neurons were found in both the superficial and deep nuclear regions of the subnucleus caudalis (Vc) and in the interface between the nucleus caudalis and interpolaris (Vc/Vi). Thirty-seven neurons had cutaneous receptive fields and were classified as either NS (16) or WDR (21) neurons. Repeated heat stimulation of the dental pulp sensitized and increased the number of electrically evoked potentials of tooth pulp neurons. These results provide evidence that both the Vc and Vc/Vi regions contain neurons that respond to noxious thermal stimulation of the dental pulp, and that these cells may contribute to the sensitization process associated with symptomatic pulpitis.


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