A modulatory effect of the feedback from higher visual areas to V1 in the mouse

Pasquale, Roberto De; Sherman, S. Murray

doi:10.1152/jn.01083.2012

Cited by 41 publications

(17 citation statements)

References 58 publications

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“…The positive shift in the holding current and decrease in input resistance are consistent with hyperpolarization. Thus similar to the results recently found in the visual cortex (De Pasquale and Sherman, 2013), group II mGluRs continue to hyperpolarize barrel neurons in adult mice.…”

Section: Resultssupporting

confidence: 90%

Developmental decline in modulation of glutamatergic synapses in layer IV of the barrel cortex by group II metabotropic glutamate receptors

Mateo¹,

Porter²

2015

Neuroscience

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Previously, we demonstrated that group II mGluRs reduce glutamate release from thalamocortical synapses during early postnatal development (P7–11). To further examine the role of group II mGluRs in the modulation of somatosensory circuitry, we determined whether group II mGluRs continue to modulate thalamocortical synapses until adulthood and whether these receptors also modulate intra-cortical synapses in the barrel cortex. To address these issues, we examined the effect of the group II mGluR agonists on thalamocortical EPSCs and intra-barrel EPSCs in slices from animals of different ages (P7–53). We found that the depression of thalamocortical EPSCs by stimulation group II mGluRs rapidly declined after the second postnatal week. In contrast, adenosine continued to depress thalamocortical EPSCs via a presynaptic mechanism in young adult mice (P30–50). Activation group II mGluRs also reduced intra-barrel EPSCs through a postsynaptic mechanism in young mice (P7–11). Similar to the thalamocortical synapses, the group II mGluR modulation of intra-barrel excitatory synapses declined with development. In young adult animals (P30–50), group II mGluR stimulation had little effect on intra-barrel EPSCs but did hyperpolarize the neurons. Together our results demonstrate that group II mGluRs modulate barrel cortex circuitry by presynaptic and postsynaptic mechanisms depending on the source of the synapse and that this modulation declines with development.

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Section: Resultssupporting

confidence: 90%

Developmental decline in modulation of glutamatergic synapses in layer IV of the barrel cortex by group II metabotropic glutamate receptors

Mateo¹,

Porter²

2015

Neuroscience

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“…Examples of such modulation by class 2 inputs include control of tonic versus burst firing mode of thalamic relay cells (29,30) and affecting the EPSP amplitudes of class 1 inputs (1,(31)(32)(33)(34)(35). Also consistent with this modulatory role for class 2 inputs are in vivo studies showing that optogenetic manipulation of the class 2 corticogeniculate pathway from cortical layer 6 shows that gain control is one of its main roles (36,37).…”

Section: Discussionmentioning

confidence: 80%

Synaptic properties of the lemniscal and paralemniscal pathways to the mouse somatosensory thalamus

Petrof

Viaene

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Somatosensory information is thought to arrive in thalamus through two glutamatergic routes called the lemniscal and paralemniscal pathways via the ventral posterior medial (VPm) and posterior medial (POm) nuclei. Here we challenge the view that these pathways functionally represent parallel information routes. Using electrical stimulation and an optogenetic approach in brain slices from the mouse, we investigated the synaptic properties of the lemniscal and paralemniscal input to VPm and POm. Stimulation of the lemniscal pathway produced class 1, or "driver," responses in VPm relay cells, which is consistent with this being an informationbearing channel. However, stimulation of the paralemniscal pathway produced two distinct types of responses in POm relay cells: class 1 (driver) responses in 29% of the cells, and class 2, or "modulator," responses in the rest. Our data suggest that, unlike the lemniscal pathway, the paralemniscal one is not homogenous and that it is primarily modulatory. This finding requires major rethinking regarding the routes of somatosensory information to cortex and suggests that the paralemniscal route is chiefly involved in modulatory functions rather than simply being an information route parallel to the lemniscal channel.driver | modulator | glutamatergic | ventral posterior medial nucleus | posterior medial nucleus B efore reaching the cortex, all sensory information except olfaction is relayed by the thalamus. For somatosensory information, there appear to be two potential routes of such information flow, which have been termed "lemniscal" and "paralemniscal." Regarding the trigeminal components of these, the lemniscal route is represented by the pathway from the principal and spinal nuclei of the Vth nerve (PrV and SpV, respectively) via the medial lemniscus (ML) through VPm, whereas the paralemniscal route is represented by the pathway originating mostly from SpV through POm. However, exactly how these circuits function depends critically on the nature of the underlying synapses. These inputs to thalamus and from thalamus to cortex are glutamatergic, meaning that they use glutamate as a neurotransmitter. Recent work has made it clear that glutamatergic inputs in thalamus and cortex are heterogeneous and can be divided into at least two types, known as class 1 (or driver) and class 2 (or modulator) (1-3). It has been suggested that the class 1 inputs carry the main information between neuronal regions and that the class 2 inputs provide a modulatory role, mainly affecting how class 1 inputs are processed (reviewed in refs. 4-6; see also Discussion). Thus, identifying which type of glutamatergic synapses are involved in the lemniscal and paralemniscal pathways could help clarify whether they represent parallel information routes or whether some other functional explanation is more plausible.To this end, we used slice preparations in which we could use a combination of electrical stimulation and optogenetics to activate lemniscal or paralemniscal inputs to patched cells in VPm and P...

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“…This conclusion should be considered in the context of prior work that shows that activation of certain glutamatergic inputs also downregulates glutamatergic circuits, likewise through activation of mGluRs, although evidence from various sources indicates both presynaptic and postsynaptic involvement of both group I and group II mGluRs in this latter result (De Pasquale and Sherman 2011, 2012, 2013Lee and Sherman 2009a,b). It is interesting in this regard that the available evidence involving a number of examples indicates that activation of the relevant mGluRs always leads to a reduction of synaptic transmission and not an increase.…”

Section: Bimentioning

confidence: 75%

“…We adopted our previously described procedures (De Pasquale and Sherman 2011, 2012, 2013Lam and Sherman 2005;Lee and Sherman 2008;Reichova and Sherman 2004;Theyel et al 2010); these are briefly summarized below. All procedures were approved by the Institutional Animal Care and Use Committee of the University of Chicago.…”

Section: Methodsmentioning

confidence: 99%

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Modulatory effects of activation of metabotropic glutamate receptors on GABAergic circuits in the mouse cortex

Liu

Petrof

Sherman

2014

Journal of Neurophysiology

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Liu T, Petrof I, Sherman SM. Modulatory effects of activation of metabotropic glutamate receptors on GABAergic circuits in the mouse cortex. J Neurophysiol 111: 2287-2297, 2014. First published March 12, 2014 doi:10.1152/jn.00730.2013.-Metabotropic glutamate receptors (mGluRs) have a ubiquitous distribution in the central nervous system and often serve to regulate the release of neurotransmitters. We have previously shown that activation of both presynaptic and postsynaptic mGluRs can affect the gain of glutamatergic inputs in both thalamus and cortex. In the present study, we sought to determine the effect of mGluR activation on GABAergic inputs in cortex. Using whole cell recordings in a mouse slice preparation of either primary visual or auditory cortex (V1 or A1), we tested the effects on mGluRs by applying various agonists to the slice. Two pathways were tested in each area: the GABAergic inputs in layers 2/3 activated from layer 4 and the GABAergic inputs in layer 4 activated from adjacent layer 4. In both of these pathways, we found that activation of mGluRs significantly reduced the amplitude of the evoked inhibitory postsynaptic currents. Because the effects were not blocked by the addition of GDP␤S to the recording electrode, and because mGluR agonists did not affect responses to photostimulation of GABA in a low-Ca 2ϩ and high-Mg 2ϩ bathing solution, we concluded this reduction was due to activation of presynaptic mGluRs. Furthermore, using specific mGluR agonists, we found that group II mGluRs, but not group I mGluRs, were involved in these modulatory effects. Because similar results were found in both pathways in V1 and A1, a possible cortical pattern for these effects is suggested. cortical circuit; GABA; IPSC; mGluR; modulation METABOTROPIC GLUTAMATE RECEPTORS (mGluRs) are G proteincoupled receptors found in many areas of the mammalian brain (Hollmann and Heinemann 1994). Previous work from our laboratory has shown that activation of mGluRs either by agonist application or by stimulation of certain glutamatergic inputs reduces the gain of synaptic transmission in other glutamatergic inputs. Both presynaptic and postsynaptic mGluRs have been implicated in this phenomenon in various combinations [reviewed in Sherman (2014)].Recent studies have indicated the existence of mGluRs on GABAergic terminals, suggesting the possibility that activation of these receptors can modulate GABA release (Cartmell and Schoepp 2000;Pinheiro and Mulle 2008;Schoepp 2001). However, studies that tested this idea have produced a range of results. Activation of group II mGluRs has been shown to suppress GABAergic responses in hippocampus (Jouvenceau et al. 1995;Liu et al. 1993 Given the importance of GABAergic circuitry in cortex (Anderson et al. 2000;DeFelipe 1993;Ferster and Miller 2000;Haglund et al. 1992; Hamberger and van Gelder 1993;Hirsch and Martinez 2006;Marco et al. 1996;Monier et al. 2003;Sherwin 1999;Wood et al. 1979) and given the widespread presence of mGluRs in cortex, we sought to investigate the effects of...

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A modulatory effect of the feedback from higher visual areas to V1 in the mouse

Abstract: De Pasquale R, Sherman SM. A modulatory effect of the feedback from higher visual areas to V1 in the mouse.

Cited by 41 publications

References 58 publications

Developmental decline in modulation of glutamatergic synapses in layer IV of the barrel cortex by group II metabotropic glutamate receptors

Developmental decline in modulation of glutamatergic synapses in layer IV of the barrel cortex by group II metabotropic glutamate receptors

Synaptic properties of the lemniscal and paralemniscal pathways to the mouse somatosensory thalamus

Modulatory effects of activation of metabotropic glutamate receptors on GABAergic circuits in the mouse cortex

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