Dynamic changes of rodent somatosensory barrel cortex are correlated with learning a novel conditioned stimulus

Abstract

Long JD 2nd, Carmena JM. Dynamic changes of rodent somatosensory barrel cortex are correlated with learning a novel conditioned stimulus. J Neurophysiol 109: 2585-2595, 2013. First published March 6, 2013 doi:10.1152/jn.00553.2012.-The rodent somatosensory barrel cortex (S1bf) has proved a valuable model for studying neural plasticity in vivo. It has been observed that sensory deprivation or conditioning reorganizes sensory-driven activity within S1bf. These observations suggest a role for S1bf in somatosensory learning. This study evaluated the hypothesis that the response properties of extracellularly recorded neurons in S1bf would change as subjects learned to respond to stimulation of S1bf. Intracortical microstimulation (ICMS) of S1bf was used as a means for bypassing feedforward drive from the sensory periphery, midbrain, and thalamus while exciting local cortical networks. To separate the learning of this conditioned stimulus-conditioned response (CS-CR) from other elements of the task, we employed a cross-modal transfer schedule. Long-Evans rats were initially trained to respond to an auditory stimulus. All subjects were then implanted in both S1bfs with chronic microwire arrays for recording neural activity and delivering ICMS. Next, this association was transferred to ICMS of one hemisphere's S1bf. S1bf responded to ICMS with a brief increase in firing rate followed by a longer reduction in activity. We observed that the duration of reduced activity elicited by ICMS increased as the subjects began to respond correctly more often than expected by chance, and the magnitude of the initial positive response increased as they consolidated this CS-CR. Subsequent ICMS of the opposite S1bf revealed that this CS-CR did not generalize across hemispheres. These results suggest that a mechanism involving a single hemisphere's S1bf tunes cortical responses in concert with changes in rodent behavior during somatosensory learning.behavior; learning; microstimulation; rat; somatosensory learning THE RODENT VIBRISSA SYSTEM has proved a promising model system for investigating how the brain adaptively integrates sensory and motor information to generate perception (Diamond et al. 2008;Kleinfeld et al. 1999;Petersen 2007). Previous work has shown how the stimulus-driven responses of the vibrissa system, from the trigeminal ganglion to the somatosensory barrel cortex (S1bf), depend on the behavioral state of the animal (Leiser and Moxon 2007; Wiest and Nicolelis 2003). Specifically, the responses of S1bf neurons to whisker stimulation have been shown to vary dependent on whether the animal is anesthetized or awake (Petersen et al. 2003) and attentive or inattentive (Ferezou et al. 2007). Moreover, the functional reorganization of S1bf induced by sensory deprivation (Allen et al. 2002;Fox 2002) or aversive conditioning (Bekisz et al. 2010; Urban-Cieko et al. 2010) has demonstrated that the barrel cortex is highly plastic. Whether and how these changes in S1bf activity relate to the learning process remains unclear.The di...

Basal forebrain neuronal inhibition enables rapid behavioral stopping

“…5 ). Similar compound excitation-inhibition effects of electrical stimulation have been reported in cortical circuits 30 - 32 . If the stimulation-induced rebound BF excitation were to impact behavior, one would predict to see speeding of RTs, because BF stimulation designed to enhance BF bursting amplitude leads to faster RTs 24 .…”

Restoration of Hindlimb Movements after Complete Spinal Cord Injury Using Brain-Controlled Functional Electrical Stimulation

“…Not surprisingly, neuronal firing patterns changed as the animal learned to use the BMI control (BMI-b) and stopped pressing the pedal (BMI-o) compared to Behavioral Control (BC) as has been observed by several others (Figure 2A ; Ganguly and Carmena, 2009 ; Ganguly et al, 2011 ; Long and Carmena, 2013 ). During BC, a majority of neurons (87.5%) were responsive post-cue onset, encoding the intention to press the pedal (Manohar et al, 2012 ) but the proportion of responsive neurons decreased across experimental conditions (BMI-b: 2,279 of 2,628, 86.2%; BMI-o: 1,966 of 2,331, 84.3%; chi-square proportions test: χ 2 = 20.38, p < 0.001).…”

“…The enhanced discrimination of the response is likely due to learning the BMI task. In a recent study of somatosensory learning, Long and Carmena observed similar increases in response magnitude and decreased baseline activity in sensory barrel field neurons that were well correlated to increasing performance in novel cross-modal sensory task (Long and Carmena, 2013 ). The same phenomenon was also observed during BMI learning in a motor context in which monkeys were trained under a BMI but were switched between epochs of BMI and behavioral control within single experimental sessions (Ganguly and Carmena, 2009 ; Ganguly et al, 2011 ; Knudsen et al, 2014 ).…”

Neural Plasticity in Sensorimotor Brain–Machine Interfaces

“…Natural sensorimotor learning involves plasticity within the basal ganglia and the sensory, motor, and prefrontal cortices—brain areas that are responsible for adapting to new sensory information and associating sensory inputs with motor commands ( 143 ). Learning in a motor BMI also involves plasticity in, at a minimum, the basal ganglia and motor cortex ( 144 ), while learning to detect electrical stimulation requires (at least) plasticity in sensory cortical areas ( 145 ). However, electrical stimulation drives cortical plasticity even in the absence of any behavioral relevance ( 146 , 147 ), so learning within the context of a BMI will consist of a balance between adapting to stimulation-evoked responses, assigning stimulation-evoked responses behavioral relevance, and associating stimulation-evoked responses with motor commands.…”

“…Neurons typically respond to electrical stimulation by a short burst of excitation followed by a longer-lasting inhibition ( 117 ). After behavioral training, neurons have both a larger active response and a longer inhibitory phase compared with baseline ( 145 ). These changes show clear adaptation to novel experience.…”