A Cortical Circuit for Gain Control by Behavioral State

“Attention, for example, has long been known to alter the cortical response to sensory stimuli (Fontanini and Katz, 2008; Maunsell and Cook, 2002; Posner and Petersen, 1990).”

“By crossing Ai14 (Cre-dependent TdTomato reporter) mice with vasoactive intestinal peptide (VIP)-Cre mice (Madisen et al., 2010; Taniguchi et al., 2011), we labeled VIP-positive GABAergic neurons genetically.”

“We first examined the responses of three major inhibitory neuron classes using adeno-associated viral (AAV) transfection of floxed GCaMP6s into the specific Cre-expressing mice (Chen et al., 2013).”

“However, electrophysiology alone does not allow one to distinguish among the large variety of GABAergic neurons with distinct physiological functions (Huang et al., 2007; Markram et al., 2004).”

“While an appropriate level of inhibition is known to be important for cortical plasticity, almost all previous work on experience-dependent plasticity has focused on the role of PV neurons (Hensch, 2005).”

“VIP neurons are present in both upper and deep layers, as shown previously (Taniguchi et al., 2011).”

“Furthermore, activating SST neurons also suppresses the visual response without changing OSI (Lee et al., 2012).”

“One interesting feature of VIP neurons is that they express serotonin receptor 5HT3a receptor (Lee et al., 2010; Rudy et al., 2011).”

“It has been reported that VIP neurons in V1 strongly inhibit SSTpositive inhibitory neurons (Pfeffer et al., 2013), whose activation results in suppression of the visual response of excitatory neurons (Adesnik et al., 2012).”

“Rabies-virus-based retrograde tracing (Wickersham et al., 2007) showed that the upper layer VIP neurons in V1 receive direct input from the nucleus of the diagonal band of Broca (NDB), a cholinergic center in basal forebrain.”

“Sensory responses have long been known to be modulated by behavioral state, but the neural circuit responsible for this modulation has remained obscure (Maunsell and Cook, 2002; Niell and Stryker, 2010; Reynolds and Chelazzi, 2004; Wurtz and Mohler, 1976).”

“It has recently been shown that VIP neurons also inhibit SST neurons in prefrontal and auditory cortices and that activating VIP neurons increases auditory responses (Pi et al., 2013).”

“Recent advances in mouse genetics and in vivo imaging technology now allow one to characterize the responses of different types of inhibitory neurons in the mouse V1 in awake animals that are free to run (Dombeck et al., 2010; Harvey et al., 2012; Taniguchi et al., 2011).”

“…Stony Brook University, Stony Brook, NY 11790, USA 4Departments of Cellular and Molecular Pharmacology and Physiology, University of California, San Francisco, CA 94158, USA *Correspondence: yufu@phy.ucsf.edu (Y.F.), stryker@phy.ucsf.edu (M.P.S.) http://dx.doi.org/10.1016/j.cell.2014.01.050”

“Using an apparatus that allows the mouse to run freely on a styrofoam ball floating on air while its head is fixed in space (Dombeck et al., 2010), we recorded the trackball movement and calcium signals simultaneously using two-photon imaging of neurons loaded with Oregon Green BAPTA (OGB-1), allowing us to analyze th…”

“No fast nAChR component like that shown in layer I inhibitory neurons (Letzkus et al., 2011) was evident; our findings showed instead a response with slow kinetics resembling what has been found in ChATpositive bipolar neurons (Arroyo et al., 2012).”

“…while SST neurons are inhibited during locomotion are in good agreement with the current consensus that VIP neuronsmainly innervate SST neurons (Lee et al., 2013; Pfeffer et al., 2013; Pi et al., 2013), although different effects on SST neurons have also been reported (Polack et al., 2013).”

“It has been reported that VIP neurons in V1 strongly inhibit SSTpositive inhibitory neurons (Pfeffer et al., 2013), whose activation results in suppression of the visual response of excitatory neurons (Adesnik et al., 2012).”

“A previous study also reported that some neurons are activated during running in darkness (Keller et al., 2012).”

“In particular, some putative inhibitory neurons were modulated differently from the more typical broad-spiking excitatory neurons (Chen et al., 2008; Mitchell et al., 2007; Niell and Stryker, 2010).”

“…while SST neurons are inhibited during locomotion are in good agreement with the current consensus that VIP neuronsmainly innervate SST neurons (Lee et al., 2013; Pfeffer et al., 2013; Pi et al., 2013), although different effects on SST neurons have also been reported (Polack et al., 2013).”

“One interesting feature of VIP neurons is that they express serotonin receptor 5HT3a receptor (Lee et al., 2010; Rudy et al., 2011).”

“Furthermore, activating SST neurons also suppresses the visual response without changing OSI (Lee et al., 2012).”

“Cholinergic input has been shown to modulate several aspects of visual response, such as the shift of local-field-potential spectrum and response magnitude (Metherate et al., 1992; Rodriguez et al., 2004; Sato et al., 1987a; Sato et al., 1987b), similar to what we have observed for locomotion (Niell and Stryker, 2010).”

“, 2002; Hill and Tononi, 2005), and one salient feature of awake cortical responses is powerful inhibition (Haider et al., 2013).”

“Changes in the balance between intrinsic excitatory and inhibitory conductances have long been linked to the change of brain state (Bazhenov et al., 2002; Hill and Tononi, 2005), and one salient feature of awake cortical responses is powerful inhibition (Haider et al.”

“Sensory responses have long been known to be modulated by behavioral state, but the neural circuit responsible for this modulation has remained obscure (Maunsell and Cook, 2002; Niell and Stryker, 2010; Reynolds and Chelazzi, 2004; Wurtz and Mohler, 1976).”

“In barrel cortex the SST neurons become hyperpolarized and fire fewer action potentials during active or passive whisker stimulation, in contrast to neighboring neurons that are excited by stimulation (Gentet et al., 2012).”

“Changes in the balance between intrinsic excitatory and inhibitory conductances have long been linked to the change of brain state (Bazhenov et al., 2002; Hill and Tononi, 2005), and one salient feature of awake cortical responses is powerful inhibition (Haider et al.”

“…Stony Brook University, Stony Brook, NY 11790, USA 4Departments of Cellular and Molecular Pharmacology and Physiology, University of California, San Francisco, CA 94158, USA *Correspondence: yufu@phy.ucsf.edu (Y.F.), stryker@phy.ucsf.edu (M.P.S.) http://dx.doi.org/10.1016/j.cell.2014.01.050”

“Inhibitory neurons may alter dendritic integration of sensory signals (Huber et al., 2012; Petreanu et al., 2012; Xu et al., 2012), and different inhibitory neurons have been hypothesized to play critical roles in behavioral state-dependent modulation of sensory processing (Buia and Tiesinga, 2008).”

“However, electrophysiology alone does not allow one to distinguish among the large variety of GABAergic neurons with distinct physiological functions (Huang et al., 2007; Markram et al., 2004).”

“In particular, some putative inhibitory neurons were modulated differently from the more typical broad-spiking excitatory neurons (Chen et al., 2008; Mitchell et al., 2007; Niell and Stryker, 2010).”

“Sensory-motor integration in rodents has been studied extensively in primary somatosensory barrel cortex, in which whisker movement and sensory information are sent to different segments of the same pyramidal neuron (Crochet et al., 2011; Petreanu et al., 2012; Xu et al., 2012).”

“It has also been shown that PV neurons do not respond to ACh (Kawaguchi, 1997) and are not directly activated by stimulating basal forebrain cholinergic neurons (Alitto and Dan, 2012; Arroyo et al.”

“Furthermore, besides increasing visual responses, locomotion has been shown to relieve surround suppression (Ayaz et al., 2013).”

“Cholinergic input has been shown to modulate several aspects of visual response, such as the shift of local-field-potential spectrum and response magnitude (Metherate et al., 1992; Rodriguez et al., 2004; Sato et al., 1987a; Sato et al., 1987b), similar to what we have observed for locomotion (Niell and Stryker, 2010).”

“Cholinergic input has been shown to modulate several aspects of visual response, such as the shift of local-field-potential spectrum and response magnitude (Metherate et al., 1992; Rodriguez et al., 2004; Sato et al., 1987a; Sato et al., 1987b), similar to what we have observed for locomotion (Niell and Stryker, 2010).”

“Attention, for example, has long been known to alter the cortical response to sensory stimuli (Fontanini and Katz, 2008; Maunsell and Cook, 2002; Posner and Petersen, 1990).”

“Acetylcholine has been demonstrated to play important roles in cortical activation and attentional modulation in many systems (Hasselmo and Giocomo, 2006; Weinberger, 2007).”

“Acetylcholine has been demonstrated to play important roles in cortical activation and attentional modulation in many systems (Hasselmo and Giocomo, 2006; Weinberger, 2007).”

“The midbrain locomotor center including the pedunculopontine tegmental nucleus (PPTg) projects to multiple subcortical and cortical areas, as well as to basal forebrain (Garcia-Rill, 1991; Newman et al., 2012).”

“Attention, for example, has long been known to alter the cortical response to sensory stimuli (Fontanini and Katz, 2008; Maunsell and Cook, 2002; Posner and Petersen, 1990).”

“Some VIP neurons reside in layer I or layer I/II border, and unidentified layer I interneurons have been reported to be activated by basal forebrain stimulation through nAChRs (Alitto and Dan, 2012; Letzkus et al., 2011).”

“No fast nAChR component like that shown in layer I inhibitory neurons (Letzkus et al., 2011) was evident; our findings showed instead a response with slow kinetics resembling what has been found in ChATpositive bipolar neurons (Arroyo et al., 2012).”

“Cholinergic input has been shown to modulate several aspects of visual response, such as the shift of local-field-potential spectrum and response magnitude (Metherate et al., 1992; Rodriguez et al., 2004; Sato et al., 1987a; Sato et al., 1987b), similar to what we have observed for locomotion (Niell and Stryker, 2010).”

“Inhibitory neurons may alter dendritic integration of sensory signals (Huber et al., 2012; Petreanu et al., 2012; Xu et al., 2012), and different inhibitory neurons have been hypothesized to play critical roles in behavioral state-dependent modulation of sensory processing (Buia and Tiesinga, 2008).”

“For example, the neurons in NDB and nearby nuclei have been found to respond not only to locomotion but also to other stimuli such as females (inmalemice) andwater (Mink et al., 1983).”