Receptive field size for certain neurons in primary somatosensory cortex is determined by GABA-mediated intracortical inhibition

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)

Download Full-text

Somatosensory cortex in macaque monkeys: laminar differences in receptive field size in areas 3b and 1

Brain Research ◽

10.1016/0006-8993(85)91144-8 ◽

1985 ◽

Vol 342 (2) ◽

pp. 391-395 ◽

Cited By ~ 42

Author(s):

Mriganka Sur ◽

Preston E. Garraghty ◽

Charles J. Bruce

Keyword(s):

Receptive Field ◽

Somatosensory Cortex ◽

Field Size ◽

Macaque Monkeys ◽

Receptive Field Size

Download Full-text

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

Brain Structure and Function ◽

10.1007/s00429-021-02309-5 ◽

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.

Download Full-text

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

10.1101/2021.01.15.426783 ◽

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.

Download Full-text

ENLARGEMENT OF THE RECEPTIVE FIELD SIZE TO LOW INTENSITY MECHANICAL STIMULATION IN THE RAT SPINAL NERVE LIGATION MODEL OF NEUROPATHY

Journal of the Peripheral Nervous System ◽

10.1046/j.1529-8027.2000.00022-48.x ◽

2000 ◽

Vol 5 (4) ◽

pp. 248-248

Author(s):

R Suzuki ◽

Vk Kontinen ◽

E Matthews ◽

E Williams ◽

Ah Dickenson

Keyword(s):

Receptive Field ◽

Mechanical Stimulation ◽

Spinal Nerve ◽

Spinal Nerve Ligation ◽

Field Size ◽

Receptive Field Size ◽

Low Intensity

Download Full-text

Spatio-Temporal Subthreshold Receptive Fields in the Vibrissa Representation of Rat Primary Somatosensory Cortex

Journal of Neurophysiology ◽

10.1152/jn.1998.80.6.2882 ◽

1998 ◽

Vol 80 (6) ◽

pp. 2882-2892 ◽

Cited By ~ 214

Author(s):

Christopher I. Moore ◽

Sacha B. Nelson

Keyword(s):

Receptive Field ◽

Somatosensory Cortex ◽

Rise Time ◽

Cortical Plasticity ◽

Temporal Dynamics ◽

Receptive Fields ◽

Excitatory Input ◽

Primary Somatosensory Cortex ◽

Spatio Temporal ◽

Sensory Evoked

Moore, Christopher I. and Sacha B. Nelson. Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J. Neurophysiol. 80: 2882–2892, 1998. Whole cell recordings of synaptic responses evoked by deflection of individual vibrissa were obtained from neurons within adult rat primary somatosensory cortex. To define the spatial and temporal properties of subthreshold receptive fields, the spread, amplitude, latency to onset, rise time to half peak amplitude, and the balance of excitation and inhibition of subthreshold input were quantified. The convergence of information onto single neurons was found to be extensive: inputs were consistently evoked by vibrissa one- and two-away from the vibrissa that evoked the largest response (the “primary vibrissa”). Latency to onset, rise time, and the incidence and strength of inhibitory postsynaptic potentials (IPSPs) varied as a function of position within the receptive field and the strength of evoked excitatory input. Nonprimary vibrissae evoked smaller amplitude subthreshold responses [primary vibrissa, 9.1 ± 0.84 (SE) mV, n = 14; 1-away, 5.1 ± 0.5 mV, n = 38; 2-away, 3.7 ± 0.59 mV, n = 22; 3-away, 1.3 ± 0.70 mV, n = 8] with longer latencies (primary vibrissa, 10.8 ± 0.80 ms; 1-away, 15.0 ± 1.2 ms; 2-away, 15.7 ± 2.0 ms). Rise times were significantly faster for inputs that could evoke action potential responses (suprathreshold, 4.1 ± 1.3 ms, n = 8; subthreshold, 12.4 ± 1.5 ms, n = 61). In a subset of cells, sensory evoked IPSPs were examined by deflecting vibrissa during injection of hyperpolarizing and depolarizing current. The strongest IPSPs were evoked by the primary vibrissa ( n = 5/5), but smaller IPSPs also were evoked by nonprimary vibrissae ( n = 8/13). Inhibition peaked by 10–20 ms after the onset of the fastest excitatory input to the cortex. This pattern of inhibitory activity led to a functional reversal of the center of the receptive field and to suppression of later-arriving and slower-rising nonprimary inputs. Together, these data demonstrate that subthreshold receptive fields are on average large, and the spatio-temporal dynamics of these receptive fields vary as a function of position within the receptive field and strength of excitatory input. These findings constrain models of suprathreshold receptive field generation, multivibrissa interactions, and cortical plasticity.

Download Full-text

Receptive Field Size and Response Latency Are Correlated Within the Cat Visual Thalamus

Journal of Neurophysiology ◽

10.1152/jn.00847.2004 ◽

2005 ◽

Vol 93 (6) ◽

pp. 3537-3547 ◽

Cited By ~ 20

Author(s):

Chong Weng ◽

Chun-I Yeh ◽

Carl R. Stoelzel ◽

Jose-Manuel Alonso

Keyword(s):

Receptive Field ◽

Spatial Frequency ◽

Response Latency ◽

Time Course ◽

Frequency Tuning ◽

Receptive Fields ◽

Cortical Cell ◽

Field Size ◽

Receptive Field Size ◽

Spatial Frequency Tuning

Each point in visual space is encoded at the level of the thalamus by a group of neighboring cells with overlapping receptive fields. Here we show that the receptive fields of these cells differ in size and response latency but not at random. We have found that in the cat lateral geniculate nucleus (LGN) the receptive field size and response latency of neighboring neurons are significantly correlated: the larger the receptive field, the faster the response to visual stimuli. This correlation is widespread in LGN. It is found in groups of cells belonging to the same type (e.g., Y cells), and of different types (i.e., X and Y), within a specific layer or across different layers. These results indicate that the inputs from the multiple geniculate afferents that converge onto a cortical cell (approximately 30) are likely to arrive in a sequence determined by the receptive field size of the geniculate afferents. Recent studies have shown that the peak of the spatial frequency tuning of a cortical cell shifts toward higher frequencies as the response progresses in time. Our results are consistent with the idea that these shifts in spatial frequency tuning arise from differences in the response time course of the thalamic inputs.

Download Full-text