Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex

Abstract

The rodent primary somatosensory cortex is spontaneously active in the form of locally synchronous membrane depolarizations (UP states) separated by quiescent hyperpolarized periods (DOWN states) both under anesthesia and during quiet wakefulness. In vivo whole-cell recordings and tetrode unit recordings were combined with voltage-sensitive dye imaging to analyze the relationship of the activity of individual pyramidal neurons in layer 2͞3 to the ensemble spatiotemporal dynamics of the spontaneous depolarizations. These were either brief and localized to an area of a barrel column or occurred as propagating waves dependent on local glutamatergic synaptic transmission in layer 2͞3. Spontaneous activity inhibited the sensory responses evoked by whisker deflection, accounting almost entirely for the large trial-to-trial variability of sensory-evoked postsynaptic potentials and action potentials. Subthreshold sensory synaptic responses evoked while a cortical area was spontaneously depolarized were smaller, briefer and spatially more confined. Surprisingly, whisker deflections evoked fewer action potentials during the spontaneous depolarizations despite neurons being closer to threshold. The ongoing spontaneous activity thus regulates the amplitude and the time-dependent spread of the sensory response in layer 2͞3 barrel cortex.T he neocortex is spontaneously active. Neocortical neurons in vivo exhibit spontaneous subthreshold membrane potential changes, which can evoke spontaneous action potentials (APs). Such spontaneous activity is not only found in association cortex but is also evident in primary sensory areas. Previous studies have shown that both during slow wave sleep and during anesthesia, the brain state is characterized by low frequency, large amplitude spontaneous membrane potential changes (1-3). Dual intracellular recordings have demonstrated that such spontaneous activity can occur synchronously in nearby neurons (4). Voltage-sensitive dye (VSD) imaging has shown complex patterns of spatiotemporal dynamics of the ensemble spontaneous activity (5-7). The nature of this spontaneous activity and how it interacts with sensory responses is poorly understood.To investigate the relationship between sub-and suprathreshold membrane potential changes of individual neurons in layer 2͞3 and the surrounding network, we combined whole-cell (WC) recordings, VSD imaging, and tetrode recordings for in vivo measurements in rodent barrel cortex. Surprisingly, unlike in the anesthetized cat where spontaneous depolarization enhanced responses (6, 8, 9), here we find that both sensory-evoked postsynaptic potentials (PSPs) and sensory-evoked APs are suppressed by ongoing spontaneous activity. This spontaneous activity occurs as both brief localized depolarizations and propagating waves of glutamatergic excitation in layer 2͞3. MethodsSurgical Procedures. Wistar rats or mice C57BL6 aged P21-P35 were anesthetized with urethane (1.5-2 g/kg), ketamine (100 mg/kg)͞xylazine (20 mg/kg), or halothane (1.5-2%). Paw withdrawal, whisk...

Interaction between neocortical and hippocampal networks via slow oscillations

“…This dynamic, which has similar characteristics to the slow oscillation discussed above, depends on synaptic activity and intrinsic currents, but does not have a clear periodicity and is limited to small ensembles of cells (Mao et al, 2001;Cossart et al, 2003). Fluctuation of finite network patterns, similar to the spontaneous events, is also evoked by sensory stimulation in deeply anesthetized animals (Lampl et al, 1999;Tsodyks et al, 1999;Arieli et al, 1996;Anderson et al, 2000;Leopold et al, 2003;Petersen et al, 2003). Thus, the population dynamics of cortical networks might display a random walk between synchronous UP states in subpopulations of neurons, which seem to reflect behaviorally activated states and silence (Kenet et al, 2003).…”

“…Because sensory stimuli can trigger UP states (Petersen et al, 2003), this might explain why at least some K complexes are associated with sensory inputs in sleeping subjects (Halasz et al, 2004).…”

Mapping somatosensory connectivity in adult mice using diffusion MRI tractography and super-resolution track density imaging

“…Network tracking techniques include lesion studies, (Killackey and Fleming, 1985;Killackey and Leshin, 1975); carbocyanine dyes (1,1'-dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine Perchlorate; DiI, DiA) (Kivrak and Erzurumlu, 2013;Seehaus et al, 2013) and myelin staining (Barrera et al, 2012); these techniques are also complemented by Lenti and Adeno-associated viral vector expression of fluorescent proteins (Aronoff et al, 2010;Dittgen et al, 2004;Wimmer et al, 2010). A range of macroscopic to microscopic functional connectivity mapping techniques include functional MRI (Kim et al, 2012;Yang et al, 1996), 2-photon imaging of electrical activity using voltage-sensitive dyes (Petersen et al, 2003a;Petersen et al, 2003b) and channelrhodopsins to map neuronal connectivity have also been conducted (Paz et al, 2011;Petreanu et al, 2007).…”

Integrated Brain Circuits: Neuron-Astrocyte Interaction in Sleep-Related Rhythmogenesis

“…On a large spatial scale, these oscillations have been described as traveling waves originating at a higher probability from prefrontal regions in the sleeping human brain[36]. At smaller scales, slow oscillation activity has complex spatial dynamics[37,38]. Slow oscillations are highly synchronized in the ipsi- and controlateral hemispheres, most likely through the activation of callosal projections[39] and are not limited to neocortical regions, but are also observed in the paleocortex[40], the hippocampus[41,42], and the thalamus[43,44,45,46].…”