Independent Controls of Attentional Influences in Primary and Secondary Somatosensory Cortex

2005 ◽  
Vol 94 (6) ◽  
pp. 4094-4107 ◽  
Author(s):  
C. Elaine Chapman ◽  
El-Mehdi Meftah

The neuronal mechanisms underlying enhanced perception of tactile stimuli with directed attention were investigated using single-unit recordings from primary (S1, n = 53) and secondary (S2, n = 50) somatosensory cortex in macaque monkeys. Neuronal responses to textures scanned under the digit tips (spatial periods, SP, of 2, 3.7 or 4.7 mm) were recorded while attention was directed either to discriminating a change in texture or to the reward and also in a neutral no-task condition. Cell discharge was quantified in three periods of the trials: salient Δ texture (directed attention), postreward, and static (both cases, attention directed to the reward). S1 texture- and non-texture-sensitive cells, as well as S2 non-texture-sensitive cells, showed a modest enhancement of discharge during the salient Δ texture period (∼25%) but no change in response gain, consistent with an additive increase in neuronal responsiveness with directed attention. In contrast, S2 texture-related cells showed a larger enhancement with directed attention to salient inputs (82%) and increased response gain, suggesting that directed attention produces a multiplicative increase in S2 responsiveness. During the postreward period, and also in no-task testing, S1 texture-sensitive cells preserved their sensitivity to SP. In contrast, S2 texture-, but not non-texture-, sensitive cells showed a marked suppression of discharge and decreased gain after the discrimination response. Together, the results support the notion that S2 discharge reflects stimulus parameters in relation to ongoing behavioral demands. The results also support the existence of two independent attentional mechanisms in somatosensory cortex, one generalized (S1 and S2), and the other focused on S2 texture-related cells.

2009 ◽  
Vol 101 (5) ◽  
pp. 2649-2667 ◽  
Author(s):  
El-Mehdi Meftah ◽  
Stéphanie Bourgeon ◽  
C. Elaine Chapman

The neuronal mechanisms that contribute to tactile perception were studied using single-unit recordings from the cutaneous hand representation of primate primary (S1) and secondary (S2) somatosensory cortex. This study followed up on our recent observation that S1 and S2 neurons developed a sustained change in discharge during the instruction period of a directed-attention task. We determined the extent to which the symbolic light cues, which signaled the modality (tactile, visual) to attend and discriminate, elicited changes in discharge rate during the instructed delay (ID) period of the attention task and the functional importance of this discharge. ID responses, consisting of a sustained increase or decrease in discharge during the 2-s instruction period, were present in about 40% of the neurons in S1 and S2. ID responses in both cortical regions were very similar in most respects (frequency, sign, latency, amplitude), suggesting a common source. A major difference, however, was related to attentional modulation during the ID period: attentional influences were almost entirely restricted to S2 and these effects were always superimposed on the ID response (additive effect). These findings suggest that the underlying mechanisms for ID discharge and attention are independent. ID discharge significantly modified the initial response to the standard stimuli (competing texture and visual stimuli), usually enhancing responsiveness. We also showed that tactile detection in humans is enhanced during the ID period. Together, the results suggest that ID discharge represents a priming mechanism that prepares cortical areas to receive and process sensory inputs.


2016 ◽  
Vol 115 (4) ◽  
pp. 2105-2123 ◽  
Author(s):  
Hui-Xin Qi ◽  
Jamie L. Reed ◽  
Joao G. Franca ◽  
Neeraj Jain ◽  
Yoshinao Kajikawa ◽  
...  

In somatosensory cortex, tactile stimulation within the neuronal receptive field (RF) typically evokes a transient excitatory response with or without postexcitatory inhibition. Here, we describe neuronal responses in which stimulation on the hand is followed by suppression of the ongoing discharge. With the use of 16-channel microelectrode arrays implanted in the hand representation of primary somatosensory cortex of New World monkeys and prosimian galagos, we recorded neuronal responses from single units and neuron clusters. In 66% of our sample, neuron activity tended to display suppression of firing when regions of skin outside of the excitatory RF were stimulated. In a small proportion of neurons, single-site indentations suppressed firing without initial increases in response to any of the tested sites on the hand. Latencies of suppressive responses to skin indentation (usually 12–34 ms) were similar to excitatory response latencies. The duration of inhibition varied across neurons. Although most observations were from anesthetized animals, we also found similar neuron response properties in one awake galago. Notably, suppression of ongoing neuronal activity did not require conditioning stimuli or multi-site stimulation. The suppressive effects were generally seen following single-site skin indentations outside of the neuron's minimal RF and typically on different digits and palm pads, which have not often been studied in this context. Overall, the characteristics of widespread suppressive or inhibitory response properties with and without initial facilitative or excitatory responses add to the growing evidence that neurons in primary somatosensory cortex provide essential processing for integrating sensory stimulation from across the hand.


1993 ◽  
Vol 70 (5) ◽  
pp. 2086-2096 ◽  
Author(s):  
G. H. Duncan ◽  
M. C. Bushnell ◽  
J. L. Oliveras ◽  
N. Bastrash ◽  
N. Tremblay

1. The present study evaluates the necessity of the ventroposterior medial thalamic nucleus (VPM) for discrimination of the intensity of noxious heating, innocuous cooling, and innocuous tactile (airpuff) stimulation of the maxillary skin. 2. Two rhesus monkeys were trained to detect small differences (< 1.0 degrees C) in the intensity of noxious heat (near 46 degrees C) and innocuous cold (near 30 degrees C) as well as differences in the force of an airpuff applied to the skin over the maxilla. As a control the monkeys also detected small differences in the intensity of a white light. Lidocaine hydrochloride (2%) was microinjected into regions of thalamus where single-unit recordings had identified neuronal responses to the noxious heating and/or cooling stimuli. The effectiveness of the anesthetic blockade was monitored by multiunit recordings using microelectrodes positioned 1-3 mm from the orifice of the injection cannula. The monkey's ability to detect near-threshold changes in stimulus intensity was compared before and after each injection. 3. During six experimental sessions, single injections of 1-4 microliters lidocaine near the dorsomedial border of VPM did not significantly alter the monkey's ability to detect small changes in the intensity of noxious heat, cool, airpuff, or visual stimuli despite neurophysiological evidence that spontaneous neuronal activity was blocked within parts of VPM. 4. During three experiments, dual simultaneous microinjections of lidocaine (delivered through 2 microcannulae separated by approximately 1 mm) resulted in profound deficits in noxious heat discrimination, with lesser deficits in cool and airpuff discrimination; visual discrimination was never altered. Monitoring of adjacent microelectrodes revealed that although activity ventral to the injection sites was blocked, activity in medial thalamic nuclei, implicated in nociceptive processing, was probably not altered by these injections. 5. These data suggest that VPM is important for the perception of noxious and innocuous thermal stimuli as well as for the perception of tactile stimuli. However, considering the ineffectiveness of small single microinjections of lidocaine, it appears that some critical proportion of VPM must be inactivated to disrupt thermal or tactile discrimination, possibly because of overlapping receptive field properties of neurons in different areas of the nucleus.


2010 ◽  
Vol 104 (5) ◽  
pp. 2389-2406 ◽  
Author(s):  
Claudia Roth-Alpermann ◽  
Farzana Anjum ◽  
Robert Naumann ◽  
Michael Brecht

Cortical organization in the Etruscan shrew is of comparative interest because of its small size and because the Etruscan shrew is an amazing tactile hunter. Here we investigated cortical organization in Etruscan shrews by electrophysiological mapping. We developed an anesthesia protocol for this very small mammal in which we combined massive application of local anesthesia, very slow induction of general anesthesia, and passive cooling. Under this anesthesia regime, we characterized auditory, visual, and somatosensory cortical responses. We found that large parts of shrew cortex respond to such stimuli. Of the responsive sites, a small fraction (∼14%) responded to visual stimuli in a caudally located region. Another small fraction of sites (∼11%) responded to auditory stimuli in a centrally located region. The majority of sites (∼75%) responded to tactile stimuli. We identified two topographically organized somatosensory areas with small receptive fields referred to as putative primary somatosensory cortex and putative secondary somatosensory cortex. In a posterior-lateral region that partially overlaps with piriform cortex, we observed large somatosensory receptive fields and often polysensory responses. In an anterior-lateral region that partially overlaps with piriform cortex, we observed large unimodal somatosensory receptive fields. Our findings demonstrate a remarkable degree of tactile specialization in Etruscan shrew cortex.


2021 ◽  
Author(s):  
Aurélie Pala ◽  
Garrett B Stanley

Lateralization is a hallmark of somatosensory processing in the mammalian brain. However, in addition to their contralateral representation, unilateral tactile stimuli also modulate neuronal activity in somatosensory cortices of the ipsilateral hemisphere. The cellular organization and functional role of these ipsilateral stimulus responses in awake somatosensory cortices, especially regarding stimulus coding, are unknown. Here, we targeted silicon probe recordings to the vibrissa region of primary (S1) and secondary (S2) somatosensory cortex of awake head-fixed male and female mice while delivering ipsilateral and contralateral whisker stimuli. Ipsilateral stimuli drove larger and more reliable responses in S2 than in S1, and activated a larger fraction of stimulus-responsive neurons. Ipsilateral stimulus-responsive neurons were rare in layer 4 of S1, but were located in equal proportion across all layers in S2. Linear classifier analyses further revealed that decoding of the ipsilateral stimulus was more accurate in S2 than S1, while S1 decoded contralateral stimuli most accurately. These results reveal substantial encoding of ipsilateral stimuli in S1 and especially S2, consistent with the hypothesis that higher cortical areas may integrate tactile inputs across larger portions of space, spanning both sides of the body.


1979 ◽  
Vol 42 (6) ◽  
pp. 1538-1556 ◽  
Author(s):  
J. E. Kanz ◽  
L. B. Eberly ◽  
J. S. Cobbs ◽  
H. M. Pinsker

1. Central neuronal mechanisms of siphon withdrawal in Aplysia were studied for the first time in intact, freely behaving animals by means of population recordings from implanted whole-nerve cuff electrodes. Intracellular follow-up studies were then conducted when the same animal was reduced to a semi-intact preparation. 2. Background spontaneous activity in the siphon nerve consisted of low-frequency firing of a population of efferent units containing identified siphon motoneurons. 3. Spontaneous patterned bursts of efferent activity occurred irregularly and were associated with all-or-nothing contractions of the parapodia, gill, and siphon. Spontaneous bursts were due to centrally generated activity in the interneuron II (INT II) network, an oscillatory network with endogenous pacemaker properties. 4. In intact animals, even weak tactile stimuli to the siphon typically triggered an INTII burst shortly after the stimulus-locked efferent activity. Thus, the stimulus can phase-advance the INT II oscillator. In semi-intact preparations, short-latency INT II bursts were triggered less less frequently and required more intense stimuli. 5. With weak to moderate-intensity stimuli in intact animals, the presence of short-latency triggered INT II bursts largely determined the duration of the siphon component and amplitude of the gill component of the withdrawal reflex. 6. When stimuli were repeated over a range of interstimulus intervals (from 60 to 1 min), the likelihood of triggering a short-latency INT II burst die not change systematically. Thus, the ability of the siphon stimulus to stably entrain the all-or-none INT II component over a wide range of intervals will interact behaviorally with the decrement of the monosynaptic component of the reflex with repetition.


2019 ◽  
Author(s):  
Robert G. Law ◽  
Sarah Pugliese ◽  
Hyeyoung Shin ◽  
Danielle Sliva ◽  
Shane Lee ◽  
...  

AbstractTransient neocortical events with high spectral power in the 15–29Hz beta band are among the most reliable predictors of sensory perception: High prestimulus beta event rates in primary somatosensory lead to sensory suppression, most effective at 100–300ms prestimulus latency. However, the synaptic and neuronal mechanisms inducing beta’s perceptual effects have not been completely localized. We combined human MEG with neural modeling designed to account for these macroscale signals to interpret the cellular and circuit mechanisms that underlie the influence of beta on tactile detection. Extending prior studies, we modeled the hypothesis that higher-order thalamic bursts, sufficient for beta event generation in cortex, recruit supragranular GABAB inhibition acting on a 300ms time scale to suppress sensory information. Consistency between model and MEG data supported this hypothesis and led to a further prediction, validated in our data, that stimuli are perceived when beta events occur simultaneously with tactile stimulation. The post-event suppressive mechanism explains an array of studies that associate beta with decreased processing, while the during-event mechanism may demand a reinterpretation of the role of beta events in the context of coincident timing.Significance statementSomatosensory beta events – transient 15-29Hz oscillations in electromagnetic recordings – are thought to be generated when “top-down” bursts of spikes presumably originating in higher-order thalamus arrive in upper layers of somatosensory cortex. Physiological evidence had shown that the immediate action of these top-down projections should be excitatory; however, after a beta event, sensory perception is noticeably inhibited for approximately 300ms. The source of this post-event sensory suppression, in particular, had been unresolved. Using a detailed computational model of somatosensory cortex, we find evidence for the hypothesis that these bursts couple indirectly to GABAB inhibition in upper layers of cortex, and that beta events first briefly disinhibit sensory relay before a longer period of inhibition.


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