Chronic Suppression of Activity in Barrel Field Cortex Downregulates Sensory Responses in Contralateral Barrel Field Cortex

2005 ◽  
Vol 94 (5) ◽  
pp. 3342-3356 ◽  
Author(s):  
Lu Li ◽  
V. Rema ◽  
Ford F. Ebner

Numerous lines of evidence indicate that neural information is exchanged between the cerebral hemispheres via the corpus callosum. Unilateral ablation lesions of barrel field cortex (BFC) in adult rats induce strong suppression of background and evoked activity in the contralateral barrel cortex and significantly delay the onset of experience-dependent plasticity. The present experiments were designed to clarify the basis for these interhemispheric effects. One possibility is that degenerative events, triggered by the lesion, degrade contralateral cortical function. Another hypothesis, alone or in combination with degeneration, is that the absence of interhemispheric activity after the lesion suppresses contralateral responsiveness. The latter hypothesis was tested by placing an Alzet minipump subcutaneously and connecting it via a delivery tube to a cannula implanted over BFC. The minipump released muscimol, a GABAA receptor agonist at a rate of 1 μl/h, onto one barrel field cortex for 7 days. Then with the pump still in place, single cells were recorded in the contralateral BFC under urethan anesthesia. The data show a ∼50% reduction in principal whisker responses (D2) compared with controls, with similar reductions in responses to the D1 and D3 surround whiskers. Despite these reductions, spontaneous firing is unaffected. Fast spiking units are more sensitive to muscimol application than regular spiking units in both the response magnitude and the center/surround ratio. Effects of muscimol are also layer specific. Layer II/III and layer IV neurons decrease their responses significantly, unlike layer V neurons that fail to show significant deficits. The results indicate that reduced activity in one hemisphere alters cortical excitability in the other hemisphere in a complex manner. Surprisingly, a prominent response decrement occurs in the short-latency (3–10 ms) component of principal whisker responses, suggesting that suppression may spread to neurons dominated by thalamocortical inputs after interhemispheric connections are inactivated. Bilateral neurological impairments have been described after unilateral stroke lesions in the clinical literature.

2007 ◽  
Vol 97 (4) ◽  
pp. 2992-3003 ◽  
Author(s):  
Aren J. Borgdorff ◽  
James F. A. Poulet ◽  
Carl C. H. Petersen

The sensory responses in the barrel cortex of mice aged postnatal day (P)7–P12 evoked by a single whisker deflection are smaller in amplitude and spread over a smaller area than those measured in P13–P21 mice. However, repetitive 10-Hz stimulation or paired pulse whisker stimulation in P7–P12 mice evoked facilitating sensory responses, contrasting with the depressing sensory responses observed in P13–P21 mice. This facilitation occurred during an interval ranging 300–1,000 ms after the first stimulus and was measured using whole cell recordings, voltage-sensitive dye imaging, and calcium-sensitive dye imaging. The facilitated responses were not only larger in amplitude but also propagated over a larger cortical area. The facilitation could be blocked by local application of pharmacological agents reducing cortical excitability. Local cortical microstimulation could substitute for the first whisker stimulus to produce a facilitated sensory response. The enhanced sensory responses evoked by repetitive sensory stimuli in P7–P12 mice may contribute to the activity-dependent specification of the developing cortical circuits. In addition, the facilitating sensory responses allow long integration times for sensory processing compatible with the slow behavior of mice during early postnatal development.


2010 ◽  
Vol 104 (1) ◽  
pp. 98-107 ◽  
Author(s):  
Maria V. Popescu ◽  
Ford F. Ebner

The normal development of sensory perception in mammals depends on appropriate sensory experience between birth and maturity. Numerous reports have shown that trimming some or all of the large mystacial vibrissa (whiskers) on one side of the face after birth has a detrimental effect on the maturation of cortical function. The objective of the present study was to understand the differences that occur after unilateral whisker trimming compared with those that occur after bilateral deprivation. Physiological deficits produced by bilateral trimming (BD) of all whiskers for 2 mo after birth were compared with the deficits produced by unilateral trimming (UD) for the same period of time using extracellular recording under urethan anesthesia from single cells in rat barrel cortex. Fast spiking (FSUs) and regular spiking (RSUs) units were separated and their properties compared in four subregions identified by histological reconstructions of the electrode penetrations, namely: layer IV barrel and septum, and layers II/III above a barrel and above a septum. UD upregulated responses in layer IV septa and in layers II/III above septa and perturbed the timing of responses to whisker stimuli. After BD, nearly all responses were decreased, and poststimulus latencies were increased. Circuit changes are proposed as an argument for how inputs arising from the spared whiskers project to the undeprived cortex and, via commissural fibers, could upregulate septal responses after UD. Following BD, more global neural deficits create a signature difference in the outcome of UD and BD in rat barrel cortex.


2005 ◽  
Vol 93 (4) ◽  
pp. 1920-1934 ◽  
Author(s):  
Michael J. Higley ◽  
Diego Contreras

Characterizing input integration at the single-cell level is a critical step to understanding cortical function, particularly when sensory stimuli are represented over wide cortical areas and single cells exhibit large receptive fields. To study synaptic integration of sensory inputs, we made intracellular recordings from the barrel cortex of anesthetized rats in vivo. For each cell, we deflected the principal whisker (PW) either alone or preceded by the deflection of a single adjacent whisker (AW) at an interval of 20 or 3 ms. At the 20-ms interval in all cases, prior AW deflection significantly suppressed the PW-evoked spike output and caused the underlying synaptic response to reach a peak Vm less depolarized than that arising from PW deflection alone. The decrease in peak Vm was not attributed to hyperpolarizing inhibition but to a divisive reduction in PW-evoked PSP amplitude. The reduction in amplitude was not a result of shunting inhibition but was mostly a result of removal of the synaptic drive, or disfacilitation. When the AW–PW interval was shortened to 3 ms, spike suppression was observed in a subset of the cells studied. In most cases, a divisive reduction in synaptic response amplitude was offset by summation with the preceding AW-evoked depolarization. To determine whether suppression is a general feature of synaptic integration by barrel cortex neurons, we also characterized the interaction of responses evoked by local electrical stimulation. In contrast to the whisker data, we found that responses to paired stimulation at the same intervals produced more spikes and reached a peak Vm more depolarized than the individual responses alone, suggesting that whisker-evoked suppression is not a result of postsynaptic mechanisms. Instead, we propose that cross-whisker response suppression depends on sensory-specific mechanisms at cortical and subcortical levels.


2008 ◽  
Vol 100 (1) ◽  
pp. 358-370 ◽  
Author(s):  
Akio Hirata ◽  
Manuel A. Castro-Alamancos

In the barrel cortex of rodents, cells respond to a principal whisker (PW) and more weakly to several adjacent whiskers (AWs). Here we show that compared with PW responses, simultaneous wide-field stimulation of the PW and several AWs enhances short-latency responses and suppresses long-latency responses. Multiwhisker enhancement and suppression is first seen at the level of the cortex in layer 4 and not in the ventroposterior medial thalamus. Within the cortex, enhancement is manifested as a reduction in spike latency in layer 4 but also as an increase in spike probability in layer 2/3. Intracellular recordings revealed that multiwhisker enhancement of short-latency responses is caused by synaptic summation that can be explained by synaptic cooperativity (i.e., convergence of synaptic inputs activated by different whiskers). Conversely, multiwhisker suppression of long-latency responses is due to increased recruitment of inhibition in cortical cells. Interestingly, the ability to differentiate multiwhisker and PW responses is lost during rapid sensory adaptation caused by high-frequency whisker stimulation. The results reveal that simultaneous and temporally dispersed wide-field sensory inputs are discriminated at the level of single cells in barrel cortex with high temporal resolution, but the ability to compute this difference is highly dynamic and dependent on the level of adaptation in the thalamocortical network.


1992 ◽  
Vol 68 (4) ◽  
pp. 1345-1358 ◽  
Author(s):  
M. Armstrong-James ◽  
K. Fox ◽  
A. Das-Gupta

1. Extracellular spike recordings were made from single cells in various layers of barrel cortex in adult rats anesthetized with urethan. Response magnitude and latency differences to brief 1.14 degrees deflections of mystacial vibrissae of center (principal) and surround receptive-field vibrissae were measured. Latency differences for pairs of cells in the same penetration to stimulation of the principal vibrissa were also collected. In separate experiments the domains of layer IV cells were mapped for their influence by a single vibrissa and their latencies to this vibrissa were recorded. In all experiments precise locations of layer IV cells in each penetration were identified using dye-lesioning and cytochrome oxidase staining of tangential sections. 2. The results suggest that principal vibrissa data are relayed radially in a column of neurons before parallel relay to adjacent columns. To the principal vibrissa, layers IV and Vb neurons discharged earliest, with layers II and III on average 2 and 3 ms later, respectively. Serial relay from layers IV to III to II was suggested to be the most common event. Although layer Va cells fired next, a single-column organization is not suggested for them because differences in latency or response magnitude to their principal and immediate surround vibrissae were not significant. Layer II, III and IV cells showed no statistical difference in latency to the nearest surround vibrissa but fired significantly later than to their principal input. 3. Because, from our previous studies, surround receptive fields of barrel cells in rat S1 cortex appear to be constructed intracortically, these data suggest a parallel column-column relay for their construction. Horizontal relay between barrels occurred first within the septae between barrels. Mean intracortical transmission velocities were calculated at approximately 0.05 m/s for column-column information transfer.


2021 ◽  
Author(s):  
Mohamad Motaharinia ◽  
Kimberly Gerrow ◽  
Roobina Boghozian ◽  
Emily White ◽  
Sun-Eui Choi ◽  
...  

Abstract Stroke profoundly disrupts cortical excitability which impedes recovery, but how it affects the function of specific inhibitory interneurons, or subpopulations therein, is poorly understood. Interneurons expressing vasoactive intestinal peptide (VIP) represent an intriguing stroke target because they can regulate cortical excitability through disinhibition. Here we chemogenetically augmented VIP interneuron excitability after stroke to show that it enhances somatosensory responses and improves recovery of paw function. Using longitudinal calcium imaging, we discovered that stroke primarily disrupts the fidelity (fraction of responsive trials) and predictability of sensory responses within a subset of highly active VIP neurons. Partial recovery of responses occurred largely within these active neurons and was not accompanied by the recruitment of minimally active neurons. Importantly, chemogenetic stimulation preserved sensory response fidelity and predictability in highly active neurons. These findings provide a new depth of understanding into how stroke and prospective therapies (chemogenetics), can influence subpopulations of inhibitory interneurons.


2001 ◽  
Vol 21 (11) ◽  
pp. 3881-3894 ◽  
Author(s):  
Helen Wallace ◽  
Stanislaw Glazewski ◽  
Katherine Liming ◽  
Kevin Fox

1990 ◽  
Vol 64 (1) ◽  
pp. 3-27 ◽  
Author(s):  
M. F. Jacquin ◽  
M. R. Wiegand ◽  
W. E. Renehan

1. Spinal trigeminal (SpV) subnucleus interpolaris (SpVi) receives inputs from trigeminal (V) first- and second-order neurons, monoamine-containing brain stem nuclei, and somatosensory cortex. Prior studies suggest that SpVi receptive-field (RF) properties cannot be predicted solely on the basis of primary afferent inputs. To assess the cortico-V projection and its role in SpVi RFs, anatomic and electrophysiological experiments were conducted. 2. Phaseolus vulgaris leucoagglutinin (PHA-L) or wheat-germ-agglutinized horseradish peroxidase (WGA-HRP) were used as anterograde tracers to study cortico-V axons in 24 normal adult rats. Injections into SI barrel cortex-labeled pyramidal fibers that decussated at all levels of the V brain stem complex, though crossing fibers were most numerous in the pyramidal decussation and pons. A small number of axons projected to ipsilateral V brain stem subnuclei. PHA-L-labeled pyramidal fibers did not give rise to collaterals in their descent through the pons and medulla. 3. Heaviest terminal labeling occurred contralaterally and in the maxillary portion of caudalis laminae III-V. Moderately dense reaction product was seen in ventral portions of all other contralateral V brain stem subnuclei, as well as in laminae I and II of caudalis. Subnucleus oralis contained the least amount of label contralateral to the injection site. Ipsilateral projections were weak and most dense in principalis. 4. Cortico-V projections were topographic between matching whisker representations. Axons most commonly had longitudinal orientations and stringy shapes. Terminal boutons occurred at the ends of short collateral branches. Many of these collaterals were derived from axons that ascended through caudal V brian stem subnuclei after crossing in the lower medulla. 5. Cortico-V labeling was heavier in septal regions between single whisker representations. This “honeycomb-like” termination pattern was most pronounced in contralateral caudalis and SpVi and ipsilateral principalis. 6. In 13 other adult rats, right SI cortex was aspirated followed by single-unit recordings in left SpVi under pentobarbital sodium anesthesia. In 9 of these, chronic effects were evaluated by recording the responses of 346 left SpVi cells 4-55 days after the lesion. In the remaining four rats, acute effects were analyzed by recording the responses of 190 SpVi cells on the day of the lesion.(ABSTRACT TRUNCATED AT 400 WORDS)


2013 ◽  
Vol 109 (9) ◽  
pp. 2382-2392 ◽  
Author(s):  
Brian R. Lustig ◽  
Robert M. Friedman ◽  
Jeremy E. Winberry ◽  
Ford F. Ebner ◽  
Anna W. Roe

In rats, navigating through an environment requires continuous information about objects near the head. Sensory information such as object location and surface texture are encoded by spike firing patterns of single neurons within rat barrel cortex. Although there are many studies using single-unit electrophysiology, much less is known regarding the spatiotemporal pattern of activity of populations of neurons in barrel cortex in response to whisker stimulation. To examine cortical response at the population level, we used voltage-sensitive dye (VSD) imaging to examine ensemble spatiotemporal dynamics of barrel cortex in response to stimulation of single or two adjacent whiskers in urethane-anesthetized rats. Single whisker stimulation produced a poststimulus fluorescence response peak within 12–16 ms in the barrel corresponding to the stimulated whisker (principal whisker). This fluorescence subsequently propagated throughout the barrel field, spreading anisotropically preferentially along a barrel row. After paired whisker stimulation, the VSD signal showed sublinear summation (less than the sum of 2 single whisker stimulations), consistent with previous electrophysiological and imaging studies. Surprisingly, we observed a spatial shift in the center of activation occurring over a 10- to 20-ms period with shift magnitudes of 1–2 barrels. This shift occurred predominantly in the posteromedial direction within the barrel field. Our data thus reveal previously unreported spatiotemporal patterns of barrel cortex activation. We suggest that this nontopographical shift is consistent with known functional and anatomic asymmetries in barrel cortex and that it may provide an important insight for understanding barrel field activation during whisking behavior.


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