Combined Voltage and Calcium Epifluorescence Imaging In Vitro and In Vivo Reveals Subthreshold and Suprathreshold Dynamics of Mouse Barrel Cortex

Berger, Thomas; Borgdorff, Aren J.; Crochet, Sylvain; Neubauer, Florian; Lefort, Sandrine; Fauvet, Bruno; Férézou, Isabelle; Carleton, Alan; Lüscher, Hans‐Rudolf; Petersen, Carl C. H.

doi:10.1152/jn.01178.2006

Cited by 166 publications

(182 citation statements)

References 57 publications

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“…We showed previously in brain slices that bolus loading of L5 (either in vivo or in vitro) filled the dendrites of L5 specifically and sufficiently to give dendritic signals while the nearby neuropil in the upper layers gave no signal (15). In the same experiments, we found that EPSPs had a negligible effect on intracellular Ca 2ϩ as have others (21)(22)(23). We examined the effect of back-propagating action potentials (BPAPs) on dendritic Ca 2ϩ by applying TTX to block Na ϩ channels first to the cortical surface and then injected to L5.…”

Section: Discussionsupporting

confidence: 58%

Enhanced dendritic activity in awake rats

Murayama

Larkum

2009

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

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Almost nothing is known about dendritic activity in awake animals and even less about its relationship to behavior. The tuft dendrites of layer 5 (L5) pyramidal neurons lie in layer 1, where long-range axons from secondary thalamic nuclei and higher cortical areas arrive. This class of input is very dependent on active thalamocortical loops and activity in higher brain areas and so is likely to be heavily influenced by the conscious state of the animal. If, as has been suggested, the dendrites of pyramidal neurons actively participate in this process, dendritic activity should greatly increase in the awake state. Here, we measured calcium activity in L5 pyramidal neuron dendrites using the ''periscope'' fiberoptic system. Recordings were made in the sensorimotor cortex of awake and anesthetized rats following sensory stimulation of the hindlimb. Bi-phasic dendritic responses evoked by hindlimb stimulation were extremely dependent on brain state. In the awake state, there was a prominent slow, delayed response whose integral was on average 14-fold larger than in the anesthetized state. Moreover, the dramatic increases in dendritic activity closely correlated to the strength of subsequent hindlimb movement. These changes were confined to L5 pyramidal dendrites and were not reflected in the response of layer 2/3 (L2/3) neurons to air-puff stimuli in general (which actually decreased in the awake state). The results demonstrate that the activity of L5 pyramidal dendrites is a neural correlate of awake behavior.calcium imaging ͉ calcium spike ͉ fiberoptics ͉ layer 5 pyramidal neuron ͉ neocortex T he changes that occur at the neuronal level from the anesthetized to the awake brain states is one of the most fundamental questions remaining in neuroscience (1-3). One leading hypothesis is that during awake sensory processing, thalamo-cortical interactions involving deep-layer pyramidal neurons result in non-specific thalamic nuclei projecting feedback input to the tuft dendrites of L5 pyramidal neurons (4). It is also hypothesized that higher cortical areas (more active during conscious processing) project to the same tuft dendrites in L1 in primary sensory areas (5, 6). Both these hypotheses predict specific input to pyramidal cell dendrites during the awake state. Given the intrinsic excitability of pyramidal tuft dendrites with their ability to sustain regenerative Ca 2ϩ activity (7,8), these hypotheses also predict that dendritic activity in these neurons should increase in the awake state.So far, it has only been possible to test the effectiveness of feedback input to L1 in vitro (9, 10). In vivo recordings of dendritic calcium activity has been restricted to anesthetized animals. In these studies, there is evidence for sensory stimulusevoked dendritic Ca 2ϩ spikes in the apical dendrites (11, 12), which is, however, suppressed by powerful dendritic inhibitory mechanisms (13) that are more active during anesthesia (14). These studies also predict that dendritic activity should increase in the awake preparation; howe...

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Section: Discussionsupporting

confidence: 58%

Enhanced dendritic activity in awake rats

Murayama

Larkum

2009

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

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“…These findings suggest that resting-state BOLD activity may thus reflect synaptic input and local cortical processing rather than neuronal output. VSD activity can indicate both super-and sub-threshold voltage activity but tends to correlate best with sub-threshold membrane potential changes 61 . As such, VSD imaging as performed in this study may be particularly apt at investigating infraslow fluctuations that may underlie similar processes related to spontaneous BOLD signal fluctuations.…”

Section: Discussionmentioning

confidence: 99%

Mesoscale infraslow spontaneous membrane potential fluctuations recapitulate high-frequency activity cortical motifs

et al. 2015

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Neuroimaging of spontaneous, resting-state infraslow (o0.1 Hz) brain activity has been used to reveal the regional functional organization of the brain and may lead to the identification of novel biomarkers of neurological disease. However, these imaging studies generally rely on indirect measures of neuronal activity and the nature of the neuronal activity correlate remains unclear. Here we show, using wide-field, voltage-sensitive dye imaging, the mesoscale spatiotemporal structure and pharmacological dependence of spontaneous, infraslow cortical activity in anaesthetized and awake mice. Spontaneous infraslow activity is regionally distinct, correlates with electroencephalography and local field potential recordings, and shows bilateral symmetry between cortical hemispheres. Infraslow activity is attenuated and its functional structure abolished after treatment with voltage-gated sodium channel and glutamate receptor antagonists. Correlation analysis reveals patterns of infraslow regional connectivity that are analogous to cortical motifs observed from higher-frequency spontaneous activity and reflect the underlying framework of intracortical axonal projections.

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“…Fluorescent signals derived from VSD imaging in vivo are composed primarily of postsynaptic membrane potentials from neurons located in superficial cortical layers (Ferezou et al, 2006;Berger et al, 2007). Using this approach, we show that 3-7 d of whisker disuse in fully mature mice leads to synaptic depression in multiple cortical regions associated with processing sensory information from the deprived whisker.…”

Section: Mechanisms Of Experience-based Cortical Depressionmentioning

confidence: 98%

α4* Nicotinic Acetylcholine Receptors Modulate Experience-Based Cortical Depression in the Adult Mouse Somatosensory Cortex

Brown

Sweetnam²,

Beange³

et al. 2012

J. Neurosci.

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The molecular mechanisms that mediate experience-based changes in the function of the cerebral cortex, particularly in the adult animal, are poorly understood. Here we show using in vivo voltage-sensitive dye imaging, that whisker trimming leads to depression of whiskerevoked sensory responses in primary, secondary and associative somatosensory cortical regions. Given the importance of cholinergic neurotransmission in cognitive and sensory functions, we examined whether ␣4-containing (␣4*) nicotinic acetylcholine receptors (nAChRs) mediate cortical depression. Using knock-in mice that express YFP-tagged ␣4 nAChRs subunits, we show that whisker trimming selectively increased the number ␣4*-YFP nAChRs in layer 4 of deprived barrel columns within 24 h, which persisted until whiskers regrew. Confocal and electron microscopy revealed that these receptors were preferentially increased on the cell bodies of GABAergic neurons. To directly link these receptors with functional cortical depression, we show that depression could be induced in normal mice by topical application or micro-injection of ␣4* nAChR agonist in the somatosensory cortex. Furthermore, cortical depression could be blocked after whisker trimming with chronic infusions of an ␣4* nAChR antagonist. Collectively, these results uncover a new role for ␣4* nAChRs in regulating rapid changes in the functional responsiveness of the adult somatosensory cortex.

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Combined Voltage and Calcium Epifluorescence Imaging In Vitro and In Vivo Reveals Subthreshold and Suprathreshold Dynamics of Mouse Barrel Cortex

Cited by 166 publications

References 57 publications

Enhanced dendritic activity in awake rats

Enhanced dendritic activity in awake rats

Mesoscale infraslow spontaneous membrane potential fluctuations recapitulate high-frequency activity cortical motifs

α4* Nicotinic Acetylcholine Receptors Modulate Experience-Based Cortical Depression in the Adult Mouse Somatosensory Cortex

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