Recruitment of Local Inhibitory Networks by Horizontal Connections in Layer 2/3 of Ferret Visual Cortex

Tucker, Thomas R.; Katz, Lawrence C

doi:10.1152/jn.00868.2001

Cited by 31 publications

(12 citation statements)

References 36 publications

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“…Inhibition appears when intracortical stimulation intensity is increased and coincides with a higher firing by interneurons (Hirsch and Gilbert 1991). The emergent inhibition due to the supralinearity of neocortical horizontal connections recruiting inhibitory networks (Tucker and Katz 2003) could thus play a synchronizing role of inhibition during slow-wave sleep to promote the onset of the silent state.…”

Section: Discussionmentioning

confidence: 99%

Neocortical inhibitory activities and long-range afferents contribute to the synchronous onset of silent states of the neocortical slow oscillation

Lemieux

Chauvette

Timofeev

2015

Journal of Neurophysiology

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Lemieux M, Chauvette S, Timofeev I. Neocortical inhibitory activities and long-range afferents contribute to the synchronous onset of silent states of the neocortical slow oscillation. J Neurophysiol 113: 768-779, 2015. First published November 12, 2014 doi:10.1152/jn.00858.2013.-During slowwave sleep, neurons of the thalamocortical network are engaged in a slow oscillation (Ͻ1 Hz), which consists of an alternation between the active and the silent states. Several studies have provided insights on the transition from the silent, which are essentially periods of disfacilitation, to the active states. However, the conditions leading to the synchronous onset of the silent state remain elusive. We hypothesized that a synchronous input to local inhibitory neurons could contribute to the transition to the silent state in the cat suprasylvian gyrus during natural sleep and under ketamine-xylazine anesthesia. After partial and complete deafferentation of the cortex, we found that the silent state onset was more variable among remote sites. We found that the transition to the silent state was preceded by a reduction in excitatory postsynaptic potentials and firing probability in cortical neurons. We tested the impact of chloride-mediated inhibition in the silent-state onset. We uncovered a long-duration (100 -300 ms) inhibitory barrage occurring about 250 ms before the silent state onset in 3-6% of neurons during anesthesia and in 12-15% of cases during natural sleep. These inhibitory activities caused a decrease in cortical firing that reduced the excitatory drive in the neocortical network. That chain reaction of disfacilitation ends up on the silent state. Electrical stimuli could trigger a network silent state with a maximal efficacy in deep cortical layers. We conclude that long-range afferents to the neocortex and chloride-mediated inhibition play a role in the initiation of the silent state. slow oscillation; long-range afferents; chloride-mediated inhibition; intracellular recordings SLOW OSCILLATION IS THE HALLMARK of the slow-wave sleep but also of several anesthetics, including ketamine-xylazine (Contreras and Steriade 1995; Steriade et al.

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Section: Discussionmentioning

confidence: 99%

Neocortical inhibitory activities and long-range afferents contribute to the synchronous onset of silent states of the neocortical slow oscillation

Lemieux

Chauvette

Timofeev

2015

Journal of Neurophysiology

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“…DGZ also projects directly to S1 barrel cortex (Chapin et al, 1987;Koralek et al, 1990). Moreover, since horizontal connections in cortex including somatosensory cortex have been shown to recruit inhibitory networks under some conditions (Tucker and Katz, 2003;Pluto et al, 2005;Keniston et al, 2010), it is possible that the projections from the DGZ to barrel cortex terminate on inhibitory FSUs that could cause subthreshold changes leading to an increased excitability in inhibitory neurons. Thus, this model predicts that the click component of the CS stimulus would activate the DGZ, which could increase the excitability of the FSUs in barrel cortex via corticocortical connections leading to a suppression of firing in the longer latency component of the barrel field responses.…”

Section: Discussionmentioning

confidence: 99%

Cross-Sensory Modulation of Primary Sensory Cortex Is Developmentally Regulated by Early Sensory Experience

Ghoshal¹,

Tomarken²,

Ebner³

2011

J. Neurosci.

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The presence of cross-sensory influences on neuronal responses in primary sensory cortex has been observed previously using several different methods. To test this idea in rat S1 barrel cortex, we hypothesized that auditory stimuli combined with whisker stimulation ("cross-sensory" stimuli) may modify response levels to whisker stimulation. Since the brain has been shown to have a remarkable capacity to be modified by early postnatal sensory activity, manipulating postnatal sensory experiences would be predicted to alter the degree of cross-sensory interactions. To test these ideas, we raised rats with or without whisker deprivation and with or without postnatal exposure to repeated auditory clicks. We recorded extracellular responses under urethane anesthesia from barrel cortex neurons in response to principal whisker stimulation alone, to auditory click stimulation alone, or to a cross-sensory stimulus. The responses were compared statistically across different stimulus conditions and across different rearing groups. Barrel neurons did not generate action potentials in response to auditory click stimuli alone in any rearing group. However, in cross-sensory stimulus conditions the response magnitude was facilitated in the 0 -15 ms post-whisker-stimulus epoch in all rearing conditions, whereas modulation of response magnitude in a later 15-30 ms post-whisker-stimulus epoch was significantly different in each rearing condition. The most significant cross-sensory effect occurred in rats that were simultaneously whisker deprived and click reared. We conclude that there is a modulatory type of cross-sensory auditory influence on normal S1 barrel cortex, which can be enhanced by early postnatal experiences.

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“…The network activation is controlled by neuromodulators, such as acetylcholine, or by activation of metabotropic glutamate receptors [78]. It depends also on the extent of the chemical and gap-junction couplings within local networks [1] and, possibly, on longer range connections between different local networks [83,84]. So a IV may reflect a combination of physiological parameters.…”

Section: Discussionmentioning

confidence: 99%

Inhibitory synchrony as a mechanism for attentional gain modulation

Tiesinga¹,

Fellous²,

Salinas³

et al. 2004

Journal of Physiology-Paris

138

116

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Recordings from area V4 of monkeys have revealed that when the focus of attention is on a visual stimulus within the receptive field of a cortical neuron, two distinct changes can occur: The firing rate of the neuron can change and there can be an increase in the coherence between spikes and the local field potential (LFP) in the gamma-frequency range (30-50 Hz). The hypothesis explored here is that these observed effects of attention could be a consequence of changes in the synchrony of local interneuron networks. We performed computer simulations of a Hodgkin-Huxley type neuron driven by a constant depolarizing current, I, representing visual stimulation and a modulatory inhibitory input representing the effects of attention via local interneuron networks. We observed that the neuronÕs firing rate and the coherence of its output spike train with the synaptic inputs was modulated by the degree of synchrony of the inhibitory inputs. When inhibitory synchrony increased, the coherence of spiking model neurons with the synaptic input increased, but the firing rate either increased or remained the same. The mean number of synchronous inhibitory inputs was a key determinant of the shape of the firing rate versus current (f-I) curves. For a large number of inhibitory inputs ($50), the f-I curve saturated for large I and an increase in input synchrony resulted in a shift of sensitivity-the model neuron responded to weaker inputs I. For a small number ($10), the f-I curves were non-saturating and an increase in input synchrony led to an increase in the gain of the response-the firing rate in response to the same input was multiplied by an approximately constant factor. The firing rate modulation with inhibitory synchrony was highest when the input network oscillated in the gamma frequency range. Thus, the observed changes in firing rate and coherence of neurons in the visual cortex could be controlled by top-down inputs that regulated the coherence in the activity of a local inhibitory network discharging at gamma frequencies.

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Recruitment of Local Inhibitory Networks by Horizontal Connections in Layer 2/3 of Ferret Visual Cortex

Cited by 31 publications

References 36 publications

Neocortical inhibitory activities and long-range afferents contribute to the synchronous onset of silent states of the neocortical slow oscillation

Neocortical inhibitory activities and long-range afferents contribute to the synchronous onset of silent states of the neocortical slow oscillation

Cross-Sensory Modulation of Primary Sensory Cortex Is Developmentally Regulated by Early Sensory Experience

Inhibitory synchrony as a mechanism for attentional gain modulation

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