The effects of acetylcholine on response properties of cat somatosensory cortical neurons

1988 ◽  
Vol 59 (4) ◽  
pp. 1231-1252 ◽  
Author(s):  
R. Metherate ◽  
N. Tremblay ◽  
R. W. Dykes
Keyword(s):  
Receptive Field ◽  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Field Size ◽  
Single Neurons ◽  
Cortical Layers ◽  
Thalamic Stimulation ◽  
A Cell ◽  
Behavioral States ◽  
Stimulation Of

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.

Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons

1984 ◽  
Vol 52 (6) ◽  
pp. 1066-1093 ◽  
Author(s):  
R. W. Dykes ◽  
P. Landry ◽  
R. Metherate ◽  
T. P. Hicks
Keyword(s):  
Receptive Field ◽  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Receptive Fields ◽  
Field Size ◽  
Primary Somatosensory Cortex ◽  
Gamma Aminobutyric Acid ◽  
Receptive Field Size ◽  
Thalamic Stimulation ◽  
Somatosensory Neurons

Extracellular recordings of 209 neurons were obtained with carbon fiber-containing multibarrel micropipettes. The cells were isolated in the primary somatosensory cortex of cats anesthetized with barbiturate and classified according to the nature of their response to natural stimuli, the nature of the surrounding multiunit responses to the same stimuli, the response to thalamic stimulation, and their depth in the cortex. To study factors controlling the excitability of somatosensory neurons, their receptive fields were examined in the presence of iontophoretically administered gamma-aminobutyric acid (GABA), glutamate, and bicuculline methiodide (BMI). Even when the neurons were depolarized to perithreshold levels with glutamate, or when local inhibitory influences mediated by GABA were antagonized by BMI, the apparent specificity for one class of afferent input was maintained. Neurons responding to stimulation of either cutaneous or deep receptors maintained their modality specificity, and neurons in cutaneous rapidly adapting regions never took on slowly adapting properties. When ejected at currents that did not elicit action potentials, glutamate lowered the threshold for activation by cutaneous stimuli but did not enlarge the receptive field. With larger ejecting currents, the neurons developed an on-going discharge, but even at these higher doses, glutamate did not produce an increase in the receptive-field size. Some neurons in regions of cortex exhibiting slowly adapting multiunit responses were relatively insensitive to glutamate. These cells required four to five times more glutamate to evoke discharges than did most neurons. Other cells, previously unresponsive to somatic stimuli, could be shown to possess distinct cutaneous receptive fields when either glutamate or BMI was ejected in their vicinity. Iontophoretically administered BMI altered the firing pattern of somatosensory neurons, causing them to discharge in bursts of 3-15 impulses. BMI enlarged the receptive-field size of neurons in regions displaying rapidly adapting multiunit background discharges but not in those regions with slowly adapting multiunit discharges. This differential effect of BMI, suggesting that GABA controls receptive-field size in rapidly adapting regions, also indicates that neurons in rapidly adapting regions differ pharmacologically from those in other submodality regions. In all cortical regions, BMI blocked the poststimulus inhibitory period that normally followed thalamic stimulation.(ABSTRACT TRUNCATED AT 400 WORDS)

Two-dimensional receptive-field organization in striate cortical neurons of the cat

1994 ◽  
Vol 11 (4) ◽  
pp. 703-720 ◽  
Author(s):  
Ming Sun ◽  
A. B. Bonds
Keyword(s):  
Receptive Field ◽  
Cortical Neurons ◽  
Ocular Dominance ◽  
Receptive Fields ◽  
Field Size ◽  
Two Dimensional ◽  
Cortical Layers ◽  
Field Organization ◽  
Receptive Field Organization ◽  
Cortical Receptive Fields

AbstractThe two-dimensional organization of receptive fields (RFs) of 44 cells in the cat visual cortex and four cells from the cat LGN was measured by stimulation with either dots or bars of light. The light bars were presented in different positions and orientations centered on the RFs. The RFs found were arbitrarily divided into four general types: Punctate, resembling DOG filters (11%); those resembling Gabor filters (9%); elongate (36%); and multipeaked-type (44%). Elongate RFs, usually found in simple cells, could show more than one excitatory band or bifurcation of excitatory regions. Although regions inhibitory to a given stimulus transition (e.g. ON) often coincided with regions excitatory to the opposite transition (e.g. OFF), this was by no means the rule. Measurements were highly repeatable and stable over periods of at least 1 h. A comparison between measurements made with dots and with bars showed reasonable matches in about 40% of the cases. In general, bar-based measurements revealed larger RFs with more structure, especially with respect to inhibitory regions. Inactivation of lower cortical layers (V-VI) by local GABA injection was found to reduce sharpness of detail and to increase both receptive-field size and noise in upper layer cells, suggesting vertically organized RF mechanisms. Across the population, some cells bore close resemblance to theoretically proposed filters, while others had a complexity that was clearly not generalizable, to the extent that they seemed more suited to detection of specific structures. We would speculate that the broadly varying forms of cat cortical receptive fields result from developmental processes akin to those that form ocular-dominance columns, but on a smaller scale.

Transient and prolonged effects of acetylcholine on responsiveness of cat somatosensory cortical neurons

1988 ◽  
Vol 59 (4) ◽  
pp. 1253-1276 ◽  
Author(s):  
R. Metherate ◽  
N. Tremblay ◽  
R. W. Dykes
Keyword(s):  
Receptive Field ◽  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Receptive Fields ◽  
Fixed Dose ◽  
Cortical Layers ◽  
Afferent Inputs ◽  
Time Periods ◽  
Layer I ◽  
Layer Vi

1. Two-hundred and seven neurons were examined for changes in their responsiveness during the iontophoretic administration of acetylcholine (ACh) in barbiturate-anesthetized cats. 2. The laminar locations of 78 cells were determined. Cholinoceptive neurons were found in all cortical layers and ranged from 50% of the cells tested in layer I to 78% in layer VI. 3. When the responsiveness of a neuron was measured by the magnitude of the discharge generated by a fixed dose of glutamate, 30 of 47 cases (64%) were potentiated, and 4 (8%) were depressed when ACh was administered during glutamate-induced excitation. 4. ACh administered during glutamate excitation was significantly more effective in altering neuronal responsiveness than was ACh administered alone (P less than 0.001). 5. When the responsiveness of a neuron was measured by the magnitude of the discharge generated by a standard somatic stimulus applied to the receptive field, 42 of 52 cases (81%) were potentiated during ACh application. This was again different from ACh treatment alone where only 4 of 27 tests (15%) resulted in subsequent enhancement of the response to somatic stimuli. 6. ACh generally increased the responsiveness of neurons with peripheral receptive fields and caused the appearance of a receptive field in some cells lacking one. 7. In many cases the changes in excitability, as measured by responses either to glutamate or to somatic stimulation, remained for prolonged time periods. When glutamate was used to test excitability, 34% (16 of 47) of the enhancements lasted more than 5 min. When somatic stimuli were used 29% (15 of 52) lasted more than 5 min. With both measures some neurons still displayed enhanced responses more than 1 h after the treatment with ACh. 8. ACh appears to act as a permissive agent that allows modification of the effectiveness with which previously existing afferent inputs drive somatosensory cortical neurons. 9. This mechanism to alter neuronal responsiveness has many of the characteristics necessary to account for the reorganization observed in somatosensory cortex following alterations in its afferent drive and may be related to some forms of learning and memory.

scholarly journals A touch of hierarchy: population receptive fields reveal fingertip integration in Brodmann areas in human primary somatosensory cortex

2021 ◽  
Author(s):  
W. Schellekens ◽  
M. Thio ◽  
S. Badde ◽  
J. Winawer ◽  
N. Ramsey ◽  
...  
Keyword(s):  
Receptive Field ◽  
Somatosensory Cortex ◽  
Receptive Fields ◽  
Body Part ◽  
Field Size ◽  
Primary Somatosensory Cortex ◽  
Vibrotactile Stimulation ◽  
Brodmann Areas ◽  
Functional Hierarchy ◽  
Stimulation Of

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.

scholarly journals A touch of hierarchy. Population Receptive Fields reveal fingertip integration in Brodmann areas in human primary somatosensory cortex

2021 ◽  
Author(s):  
W. Schellekens ◽  
M. Thio ◽  
S. Badde ◽  
J. Winawer ◽  
N. Ramsey ◽  
...  
Keyword(s):  
Receptive Field ◽  
Somatosensory Cortex ◽  
Receptive Fields ◽  
Body Part ◽  
Field Size ◽  
Primary Somatosensory Cortex ◽  
Vibrotactile Stimulation ◽  
Brodmann Areas ◽  
Functional Hierarchy ◽  
Stimulation Of

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 3 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 0.5s 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.

Changes in the response properties of neurons in the ventroposterior lateral thalamic nucleus of the raccoon after peripheral deafferentation

1996 ◽  
Vol 75 (6) ◽  
pp. 2441-2450 ◽  
Author(s):  
D. D. Rasmusson
Keyword(s):  
Receptive Field ◽  
Thalamic Nucleus ◽  
Receptive Fields ◽  
Field Size ◽  
Mechanical Stimuli ◽  
Sensory Pathways ◽  
Average Latency ◽  
Somatotopic Map ◽  
Almost All ◽  
Stimulation Of

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.

Intrinsic discharge patterns and somatosensory inputs for neurons in raccoon primary somatosensory cortex

1994 ◽  
Vol 72 (6) ◽  
pp. 2827-2839 ◽  
Author(s):  
P. J. Istvan ◽  
P. Zarzecki
Keyword(s):  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Primary Somatosensory Cortex ◽  
Membrane Properties ◽  
Postsynaptic Potentials ◽  
Synaptic Inputs ◽  
Ionic Conductances ◽  
Discharge Patterns ◽  
Intrinsic Membrane Properties ◽  
Stimulation Of

1. Discharge patterns of neurons are regulated by synaptic inputs and by intrinsic membrane properties such as their complement of ionic conductances. Discharge patterns evoked by synaptic inputs are often used to identify the source and modality of sensory input. However, the interpretation of these discharge patterns may be complicated if different neurons respond to the same synaptic input with a variety of discharge patterns due to differences in intrinsic membrane properties. The purposes of this study were 1) to investigate intrinsic discharge patterns of neurons in primary somatosensory cortex of raccoon in vivo and 2) to use somatosensory postsynaptic potentials evoked by stimulation of forepaw digits to determine thalamocortical connectivity for the same neurons. 2. Conventional intracellular recordings with sharp electrodes were made from 121 neurons in the cortical representation of glabrous skin of digit four (d4). Intracellular injection of identical current pulses (100-120 ms in duration) elicited various patterns of discharge in different neurons. Neurons were classified on the basis of these intrinsic patterns of discharge, rates of spike adaptation, and characteristics of spike waveforms. Three main groups were identified: regular spiking (RS) neurons, intrinsic bursting (IB) neurons, and fast spiking (FS) neurons. Subclasses were identified for the RS and IB groups. 3. Neurons were tested for somatosensory inputs by stimulating electrically d3, d4, and d5. Excitatory postsynaptic potentials (EPSPs) were elicited in 100% of the neurons by electrical stimulation of d4, the "on-focus" digit. EPSPs were usually followed by inhibitory postsynaptic potentials (IPSPs). Many neurons (41%) responded with EPSP-IPSP sequences after stimulation of d3 or d5, the "off-focus" digits. 4. Latencies of somatosensory EPSPs and IPSPs were used to determine the synaptic order in the cortical circuitry of RS, IB, and FS neurons. EPSPs with monosynaptic thalamocortical latencies were recorded in RS, IB, and FS neurons. 5. We conclude that precise patterns of neural discharge in primary somatosensory cortex cannot be reliable estimates of sensory inputs reaching these neurons because patterns of discharge are so strongly influenced by intrinsic membrane properties. Ionic conductances governing patterns of neuronal discharge seem almost identical in intact cortex of raccoon, rat, and cat, and in slices of rodent cortex, because similar patterns of discharge are found. The consistency of patterns of discharge across species and types of preparation suggests that these intrinsic membrane properties are a general property of cerebral cortical neurons and should be considered when evaluation sensory coding by these neurons.

Plasticity of Bat's Central Auditory System Evoked by Focal Electric Stimulation of Auditory and/or Somatosensory Cortices

2001 ◽  
Vol 85 (3) ◽  
pp. 1078-1087 ◽  
Author(s):  
Xiaofeng Ma ◽  
Nobuo Suga
Keyword(s):  
Electrical Stimulation ◽  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Electric Stimulation ◽  
Time Course ◽  
Recovery Period ◽  
Acoustic Stimulus ◽  
Acoustic Parameter ◽  
Response Curves ◽  
Stimulation Of

Recent findings indicate that the corticofugal system would play an important role in cortical plasticity as well as collicular plasticity. To understand the role of the corticofugal system in plasticity, therefore, we studied the amount and the time course of plasticity in the inferior colliculus (IC) and auditory cortex (AC) evoked by focal electrical stimulation of the AC and also the effect of electrical stimulation of the somatosensory cortex on the plasticity evoked by the stimulation of the AC. In adult big brown bats ( Eptesicus fuscus), we made the following major findings. 1) Electric stimulation of the AC evokes best frequency (BF) shifts, i.e., shifts in frequency-response curves of collicular and cortical neurons. These BF shifts start to occur within 2 min, reach a maximum (or plateau) at 30 min, and then recover ∼180 min after a 30-min-long stimulus session. When the stimulus session is lengthened from 30 to 90 min, the plateau lasts ∼60 min, but BF shifts recover ∼180 min after the session. 2) The electric stimulation of the somatosensory cortex delivered immediately after that of the AC, as in fear conditioning, evokes a dramatic lengthening of the recovery period of the cortical BF shifts but not that of the collicular BF shift. The electric stimulation of the somatosensory cortex delivered before that of the AC, as in backward conditioning, has no effect on the collicular and cortical BF shifts. 3) Electric stimulation of the AC evokes BF shifts not only in the ipsilateral IC and AC but also in the contralateral IC and AC. BF shifts are smaller in amount and shorter in recovery time for contralateral collicular and cortical neurons than for ipsilateral ones. Our findings support the hypothesis that the AC and the corticofugal system have an intrinsic mechanism for reorganization of the IC and AC, that the reorganization is highly specific to a value of an acoustic parameter (frequency), and that the reorganization is augmented by excitation of nonauditory sensory cortex that makes the acoustic stimulus behaviorally relevant to the animal through associative learning.

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