Suppression of Hindlimb Inputs to S-I Forelimb-Stump Representation of Rats With Neonatal Forelimb Removal: GABA Receptor Blockade and Single-Cell Responses

2000 ◽  
Vol 83 (6) ◽  
pp. 3377-3387 ◽  
Author(s):  
Andrey S. Stojic ◽  
Richard D. Lane ◽  
Herbert P. Killackey ◽  
Robert W. Rhoades

Neonatal forelimb removal in rats results in the development of inappropriate hindlimb inputs in the forelimb-stump representation of primary somatosensory cortex (S-I) that are revealed when GABAA and GABAB receptor activity are blocked. Experiments carried out to date have not made clear what information is being suppressed at the level of individual neurons. In this study, three potential ways in which GABA-mediated inhibition could suppress hindlimb expression in the S-I stump representation were evaluated: silencing S-I neurons with dual stump and hindlimb receptive fields, silencing neurons with receptive fields restricted to the hindlimb alone, and/or selective silencing of hindlimb inputs to neurons that normally express a stump receptive field only. These possibilities were tested using single-unit recording techniques to evaluate the receptive fields of S-I forelimb-stump neurons before, during, and after blockade of GABA receptors with bicuculline methiodide (for GABAA) and saclofen (for GABAB). Recordings were also made from normal rats for comparison. Of 92 neurons recorded from the S-I stump representation of neonatally amputated rats, only 2.2% had receptive fields that included the hindlimb prior to GABA receptor blockade. During GABA receptor blockade, 54.3% of these cells became responsive to the hindlimb, and in all but two cases, these same neurons also expressed a stump receptive field. Most of these cells (82.0%) expressed only stump receptive fields prior to GABA receptor blockade. In 71 neurons recorded from normal rats, only 5 became responsive to the hindlimb during GABA receptor blockade. GABA receptor blockade of cortical neurons, in both normal and neonatally amputated rats, resulted in significant enlargements of receptive fields as well as the emergence of receptive fields for neurons that were normally unresponsive. GABA receptor blockade also resulted in increases in both the spontaneous activity and response magnitudes of these neurons. These data support the conclusion that GABA mechanisms generally act to specifically suppress hindlimb inputs to S-I forelimb-stump neurons that normally express a receptive field on the forelimb stump only.

2004 ◽  
Vol 92 (1) ◽  
pp. 372-379 ◽  
Author(s):  
Charles P. Pluto ◽  
Richard D. Lane ◽  
Robert W. Rhoades

In adult rats that sustained forelimb amputation on the day of birth, there are numerous multi-unit recording sites in the forelimb-stump representation of primary somatosensory cortex (SI) that also respond to cutaneous stimulation of the hindlimb when cortical receptors for GABA are blocked. These normally suppressed hindlimb inputs originate in the SI hindlimb representation and synapse in the dysgranular cortex before exciting SI forelimb-stump neurons. In our previous studies, GABA (A + B) receptor blockade was achieved by topically applying a bicuculline methiodide/saclofen solution (BMI/SAC) to the cortical surface. This treatment blocks receptors throughout SI and does not allow determination of where along the above circuit the GABA-mediated suppression of hindlimb information occurs. In this study, focal injections of BMI/SAC were delivered to three distinct cortical regions that are involved in the hindlimb-to-forelimb-stump pathway. Blocking GABA receptors in the SI hindlimb representation and in the dysgranular cortex was largely ineffective in revealing hindlimb inputs (∼10% of hindlimb inputs were revealed in both cases). In contrast, when the blockade was targeted at forelimb-stump recording sites, >80% of hindlimb inputs were revealed. Thus GABAergic interneurons within the forelimb-stump representation suppress the expression of reorganized hindlimb inputs to the region. A circuit model incorporating these and previous observations is presented and discussed.


1983 ◽  
Vol 50 (4) ◽  
pp. 838-848 ◽  
Author(s):  
P. A. Simmons ◽  
A. L. Pearlman

The receptive-field properties of neurons in the striate visual cortex of normal and reeler mutant mice were studied with single-unit recording methods in order to determine whether the connections underlying these properties are altered by the developmental abnormality in neuronal position that characterizes reeler neocortex. Neurons with a projection through the corpus callosum were selected for study because they form a physiologically identifiable class of visual cortical neurons with a characteristic distribution of receptive-field properties that can be compared for normal and reeler cortex. Transcallosal cortical neurons in area 17 near its border with area 18a were identified by antidromic stimulation delivered through bipolar electrodes in the contralateral cortex. A computer controlled the visual stimuli, data acquisition, and analysis. Transcallosal neurons were principally found in layers II-III and V in the normal cortex and in a broand band deep in the reeler cortex. These populations had similar distributions of antidromic latencies, indicating that the neurons sampled from normal and reeler cortex were taken from populations with similar axonal diameters and soma sizes. The receptive-field properties of 46 units in 22 normal mice and 28 units in 11 reeler mice were characterized. Transcallosal neurons in both normal and reeler cortex were usually binocularly responsive and dominated by input from the contralateral eye. They exhibited either nonoriented (31 and 48%, respectively) or oriented (69 and 52%) receptive fields. Tuning 10 stimulus velocity was broad, with peak velocity sensitivities ranging from 1 to 1,000 degrees/s. Directional selectivity was present in 41% of normal units ad 32% of reeler units. There was no significant difference between normal and reeler cortex in the distribution of these properties. Transcallosal neurons were also examined for the presence of an inhibitory surround by comparing their responses to moving or stationary stimuli of varying sizes. Of the tested neurons, most (11/17 in normal cortex, 6/9 in reeler) showed evidence of a decrease in response to large moving stimuli. A large proportion (16/20) of normal neurons tested with stationary flashing stimuli had some degree of surround inhibition whereas significantly fewer (5/17) neurons in reeler cortex had this property. Thus, transcallosal neurons in reeler cortex less frequently had an inhibitory surround demonstrable with stationary flashing stimuli, but this difference between normal and reeler was not apparent with a moving stimulus.(ABSTRACT TRUNCATED AT 400 WORDS)


1994 ◽  
Vol 11 (4) ◽  
pp. 703-720 ◽  
Author(s):  
Ming Sun ◽  
A. B. Bonds

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.


eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Bram-Ernst Verhoef ◽  
John HR Maunsell

Shifting attention among visual stimuli at different locations modulates neuronal responses in heterogeneous ways, depending on where those stimuli lie within the receptive fields of neurons. Yet how attention interacts with the receptive-field structure of cortical neurons remains unclear. We measured neuronal responses in area V4 while monkeys shifted their attention among stimuli placed in different locations within and around neuronal receptive fields. We found that attention interacts uniformly with the spatially-varying excitation and suppression associated with the receptive field. This interaction explained the large variability in attention modulation across neurons, and a non-additive relationship among stimulus selectivity, stimulus-induced suppression and attention modulation that has not been previously described. A spatially-tuned normalization model precisely accounted for all observed attention modulations and for the spatial summation properties of neurons. These results provide a unified account of spatial summation and attention-related modulation across both the classical receptive field and the surround.


2008 ◽  
Vol 100 (2) ◽  
pp. 646-656 ◽  
Author(s):  
Ben Scholl ◽  
Michael Wehr

Sensory deafferentation results in rapid shifts in the receptive fields of cortical neurons, but the synaptic mechanisms underlying these changes remain unknown. The rapidity of these shifts has led to the suggestion that subthreshold inputs may be unmasked by a selective loss of inhibition. To study this, we used in vivo whole cell recordings to directly measure tone-evoked excitatory and inhibitory synaptic inputs in auditory cortical neurons before and after acoustic trauma. Here we report that acute acoustic trauma disrupted the balance of excitation and inhibition by selectively increasing and reducing the strength of inhibition at different positions within the receptive field. Inhibition was abolished for frequencies far below the trauma-tone frequency but was markedly enhanced near the edges of the region of elevated peripheral threshold. These changes occurred for relatively high-level tones. These changes in inhibition led to an expansion of receptive fields but not by a simple unmasking process. Rather, membrane potential responses were delayed and prolonged throughout the receptive field by distinct interactions between synaptic excitation and inhibition. Far below the trauma-tone frequency, decreased inhibition combined with prolonged excitation led to increased responses. Near the edges of the region of elevated peripheral threshold, increased inhibition served to delay rather than abolish responses, which were driven by prolonged excitation. These results show that the rapid receptive field shifts caused by acoustic trauma are caused by distinct mechanisms at different positions within the receptive field, which depend on differential disruption of excitation and inhibition.


1983 ◽  
Vol 50 (6) ◽  
pp. 1479-1496 ◽  
Author(s):  
D. R. Kenshalo ◽  
O. Isensee

Recordings were made from single SI cortical neurons in the anesthetized macaque monkey. Each isolated cortical neuron was tested for responses to a standard series of mechanical stimuli. The stimuli included brushing the skin, pressure, and pinch. The majority of cortical neurons responded with the greatest discharge frequency to brushing the receptive field, but neurons were found in areas 3b and 1 that responded maximally to pinching the receptive field. A total of 68 cortical nociceptive neurons were examined in 10 animals. Cortical neurons that responded maximally to pinching the skin were also tested for responses to graded noxious heat pulses (from 35 to 43, 45, 47, and 50 degrees C). If the neuron failed to respond or only responded to 50 degrees C, the receptive field was also heated to temperatures of 53 and 55 degrees C. Fifty-six of the total population of nociceptive neurons were tested for responses to the complete series of noxious heat pulses: 46 (80%) exhibited a progressive increase in the discharge frequency as a function of stimulus intensity, and the spontaneous activity of two (4%) was inhibited. One population of cortical nociceptive neurons possessed restricted, contralateral receptive fields. These cells encoded the intensity of noxious mechanical and thermal stimulation. Sensitization of primary afferent nociceptors was reflected in the responses of SI cortical nociceptive neurons when the ascending series of noxious thermal stimulation was repeated. The population of cortical nociceptive neurons with restricted receptive fields exhibited no adaptation in the response during noxious heat pulses of 47 and 50 degrees C. At higher temperatures the response often continued to increase during the stimulus. The other population of cortical nociceptive neurons was found to have restricted, low-threshold receptive fields on the contralateral hindlimb and, in addition, could be activated only by intense pinching or noxious thermal stimuli delivered on any portion of the body. The stimulus-response functions obtained from noxious thermal stimulation of the contralateral hindlimb were not different from cortical nociceptive neurons with small receptive fields. However, nociceptive neurons with large receptive fields exhibited a consistent adaptation during a noxious heat pulse of 47 and 50 degrees C. Based on the response characteristics of these two populations of cortical nociceptive neurons, we conclude that neurons with small receptive fields possess the ability to provide information about the localization, the intensity, and the temporal attributes of a noxious stimulus.4+.


1986 ◽  
Vol 226 (1245) ◽  
pp. 421-444 ◽  

We assume that the mammalian neocortex is built up out of some six layers which differ in their morphology and their external connections. Intrinsic connectivity is largely excitatory, leading to a considerable amount of positive feedback. The majority of cortical neurons can be divided into two main classes: the pyramidal cells, which are said to be excitatory, and local cells (most notably the non-spiny stellate cells), which are said to be inhibitory. The form of the dendritic and axonal arborizations of both groups is discussed in detail. This results in a simplified model of the cortex as a stack of six layers with mutual connections determined by the principles of fibre anatomy. This stack can be treated as a multi-input-multi-output system by means of the linear systems theory of homogeneous layers. The detailed equations for the simulation are derived in the Appendix. The results of the simulations show that the temporal and spatial behaviour of an excitation distribution cannot be treated separately. Further, they indicate specific processing in the different layers and some independence from details of wiring. Finally, the simulation results are applied to the theory of visual receptive fields. This yields some insight into the mechanisms possibly underlying hypercomplexity, putative nonlinearities, lateral inhibition, oscillating cell responses, and velocity-dependent tuning curves.


Perception ◽  
1997 ◽  
Vol 26 (1_suppl) ◽  
pp. 262-262 ◽  
Author(s):  
E M Maximova ◽  
V V Maximov ◽  
O Y Orlov

Ganglion cells of the ON-type in the frog retina produce colour-dependent responses differing in temporal patterns (short bursts to excitation of red-sensitive cones as opposed to prolonged discharges if blue-sensitive ‘green rods’ are excited). Their gated colour opponency (Kicliter et al, 1981 Brain Research210 103 – 113; Maximov et al, 1985 Vision Research25 1037 – 1049) becomes apparent from the OFF-responses in conditions when the test stimuli are superimposed on a background of another colour. So, when blue glass is introduced in the light beam (decreasing the excitation mainly of red-sensitive cones), an OFF-response is observed, much like the response to the onset of blue light. It has been suggested that opponency in ON-cells is asymmetric, ie that the red signal reaches the blue channel with reversed sign, but not vice versa. A single-unit-recording study revealed the dependence of ON-cell responses both on the colour of stimuli presented in the centre of the receptive field and on the steady illumination of its surround. Surround illumination was found to favour OFF-responses in ON-units. In some cases even the cessation of blue light elicited an OFF-response with a discharge pattern resembling that of the onset of red light. In these cases an ON-response to yellow glass could also be obtained. These observations prove some degree of symmetry in the opponency of the red and blue channels. It is suggested that feedback from horizontal cells onto photoreceptor terminals is involved in the gated colour opponency. A circuit model that reproduces the observed phenomena is presented.


1988 ◽  
Vol 59 (4) ◽  
pp. 1253-1276 ◽  
Author(s):  
R. Metherate ◽  
N. Tremblay ◽  
R. W. Dykes

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.


2001 ◽  
Vol 85 (1) ◽  
pp. 407-413 ◽  
Author(s):  
Andrey S. Stojic ◽  
Richard D. Lane ◽  
Robert W. Rhoades

Reorganization of the primary somatosensory cortex (S-I) forelimb-stump representation of rats that sustained neonatal forelimb removal is characterized by the expression of hindlimb inputs that are revealed when cortical GABA receptors are pharmacologically blocked. Recent work has shown that the majority of these inputs are transmitted from the S-I hindlimb representation to the forelimb-stump field via an, as yet, unidentified pathway between these regions. In this study, we tested the possibility that hindlimb inputs to the S-I forelimb-stump representation of neonatally amputated rats are conveyed through an intracortical pathway between the S-I hindlimb and forelimb-stump representations that involves the intervening dysgranular cortex by transiently inactivating this area and evaluating the effect on hindlimb expression in the S-I forelimb-stump representation during GABA receptor blockade. Of 332 S-I forelimb-stump recording sites from six neonatally amputated rats, 68.3% expressed hindlimb inputs during GABA receptor blockade. Inactivation of dysgranular cortex with cobalt chloride (CoCl2) resulted in a significant decrease in the number of hindlimb responsive sites (9.5%, P < 0.001 vs. cortex during GABA receptor blockade before CoCl2 treatment). Results were also compiled from S-I forelimb recording sites from three normal rats: 14.1% of 136 sites were responsive to the hindlimb during GABA receptor blockade, and all of these responses were abolished during inactivation of dysgranular cortex with CoCl2 ( P < 0.05). These results indicate that the S-I hindlimb representation transmits inputs to the forelimb-stump field of neonatally amputated rats through a polysynaptic intracortical pathway involving dysgranular cortex. Furthermore the findings from normal rats suggest that this pathway might reflect the amplification of a neuronal circuit normally present between the two representations.


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