Dual Gamma Rhythm Generators Control Interlaminar Synchrony in Auditory Cortex

Abstract

Rhythmic activity in populations of cortical neurons accompanies, and may underlie, many aspects of primary sensory processing and short-term memory. Activity in the gamma band (30 Hz up to > 100 Hz) is associated with such cognitive tasks and is thought to provide a substrate for temporal coupling of spatially separate regions of the brain. However, such coupling requires close matching of frequencies in co-active areas, and because the nominal gamma band is so spectrally broad, it may not constitute a single underlying process. Here we show that, for inhibition-based gamma rhythms in vitro in rat neocortical slices, mechanistically distinct local circuit generators exist in different laminae of rat primary auditory cortex. A persistent, 30 – 45 Hz, gap-junction-dependent gamma rhythm dominates rhythmic activity in supragranular layers 2/3, whereas a tonic depolarization-dependent, 50 – 80 Hz, pyramidal/interneuron gamma rhythm is expressed in granular layer 4 with strong glutamatergic excitation. As a consequence, altering the degree of excitation of the auditory cortex causes bifurcation in the gamma frequency spectrum and can effectively switch temporal control of layer 5 from supragranular to granular layers. Computational modeling predicts the pattern of interlaminar connections may help to stabilize this bifurcation. The data suggest that different strategies are used by primary auditory cortex to represent weak and strong inputs, with principal cell firing rate becoming increasingly important as excitation strength increases.

GABA B receptor-mediated, layer-specific synaptic plasticity reorganizes gamma-frequency neocortical response to stimulation

“…Layer 2/3 neurons are strongly connected to layer 5 neurons (38) so we need also to consider any changes in deeper layers with respect to the above layer 2/3 changes. Layer 5 local circuits (at least in auditory cortex) do not appear to support gamma rhythm generation alone (24) and, in contrast to the superficial layers, receive a predominantly inhibitory input from layer 4 (18). No change in layer 5 EPSP strength was seen in the present study.…”

“…It has been shown that the patterns of postsynaptic excitatory activity in layer 5 pyramidal cells needed to generate inhibitory input plasticityshort bursts of action potentials-need not also modify excitatory input (i.e., inhibitory synaptic potentiation onto pyramidal cells can occur without concomitant excitatory plasticity as seen in the present experiments) (45). Such a pattern of burst outputs is common in this neuron subtype during gamma rhythms in auditory cortex (24). Interestingly, this form of inhibitory synaptic plasticity did not require precise timing of pre-and postsynaptic excitatory neuronal spiking (46), but potently narrowed the integration window for input summation and enhanced output temporal precision once established (45,46).…”

Theta-associated high-frequency oscillations (110–160Hz) in the hippocampus and neocortex

“…Both terminologies are appropriate as long as it becomes clear that there are (at least) two other independent slower gamma oscillations <100 Hz in the hippocampus (in this convention, the slow gamma associated with CA3, and the middle gamma associated with mEC). Similar distinctions do possibly apply to neocortical areas such as the mEC (Middleton et al, 2008) and the auditory cortex (Ainsworth et al, 2011; see also Whittington et al, 2010). Calling HFOs ''gamma oscillations'' may be confusing because the latter term has been typically employed to denote an inhibition dependent rhythm (Whittington et al, 2000).…”

Beyond the Connectome: The Dynome

“…The amount of reproducible temporal structure is astonishing, and the task of charting such structure is by no means finished. Structure found in vitro includes: Multiple mechanistically different versions of a rhythm in the same frequency band (Roopun et al , 2010); Multiple mechanistically different rhythms in the same cortical region (Ainsworth et al , 2011); Different rhythms appearing simultaneously in different cortical layers (Oke et al , 2010; Ainsworth et al , 2012); Different effects of neuromodulators on rhythms in different brain areas (Middleton et al , 2008; Roopun et al , 2008a); Switches in temporal structure with changes in activation (Roopun et al , 2008b); Fast rhythms nested inside slower rhythms (Gloveli et al , 2005; Carracedo et al , 2013); Faster intrinsic rhythms suppressed by slower ones (Pietersen et al , 2014). Some of this structure observed in vitro has also been found in vivo .…”