Recurrent excitatory postsynaptic potentials induced by synchronized fast cortical oscillations

Abstract

Gamma frequency (about 20-70 Hz) oscillations occur during novel sensory stimulation, with tight synchrony over distances of at least 7 mm. Synchronization in the visual system has been proposed to reflect coactivation of different parts of the visual field by a single spatially extended object. We have shown that intracortical mechanisms, including spike doublet firing by interneurons, can account for tight long-range synchrony. Here we show that synchronous gamma oscillations in two sites also can cause long-lasting (>1 hr) potentiation of recurrent excitatory synapses. Synchronous oscillations lasting >400 ms in hippocampal area CA1 are associated with an increase in both excitatory postsynaptic potential (EPSP) amplitude and action potential afterhyperpolarization size. The resulting EPSPs stabilize and synchronize a prolonged beta frequency (about 10-25 Hz) oscillation. The changes in EPSP size are not expressed during non-oscillatory behavior but reappear during subsequent gamma-oscillatory events. We propose that oscillation-induced EPSPs serve as a substrate for memory, whose expression either enhances or blocks synchronization of spatially separated sites. This phenomenon thus provides a dynamical mechanism for storage and retrieval of stimulus-specific neuronal assemblies.Fast gamma-frequency oscillations in discrete neuronal populations have been linked to aspects of higher cognitive function, in particular, the selection and ''binding'' together of pertinent aspects of a sensory stimulus into a perceived whole (1, 2). The evidence for this link stems from the observation of these oscillations in cortical regions and cell populations devoted to the processing of sensory information of different modalities (3-5) and their ability to provide a framework for controlling temporal interactions between spatially discrete areas (6, 7). What still remains to be elucidated is whether this correlate of novel sensory processing is in any way linked to subsequent memory formation.The rat CA1 hippocampal region in vitro has proven useful for studying the cellular mechanisms underlying synchronized gamma-frequency oscillations. It possesses numerous synaptically interconnected inhibitory interneurons (8), which oscillate as a population at gamma frequencies on tonic excitation (9). It also has well developed recurrent inhibitory connections that allow excitatory pyramidal cells both to influence the firing of interneuron networks and to be influenced by these same inhibitory networks (Fig. 1A). In addition, a small number of recurrent excitatory connections from pyramidal cell to pyramidal cell occur (10). Most conventional models of memory formation involve the selective long-term enhancement of excitatory synaptic activity (11) to provide a favored pattern of neuronal intercommunication on representation of the original stimulus (12). Were pyramidal cell to pyramidal cell connections to be selectively inducible in CA1, not only would this suggest a possible memory mechanism, perhaps relevant to perception...

Neuronal assembly dynamics in the beta1 frequency range permits short-term memory

“…We note that this rhythm is mechanistically not the same as the PING in which the RS cells fire on almost every gamma cycle (25). Also, the RS cells of this model possess additional currents not in the previous models, but critical to sustaining the beta1 rhythm (5,6).…”

Recurrent Synaptic Input and the Timing of Gamma-Frequency-Modulated Firing of Pyramidal Cells during Neocortical “UP” States

“…Conversely, apart from several modeling studies (Whittington et al, 1997;Kopell et al, 2000;Brunel and Wang, 2003;Geisler et al, 2005;Kanamaru, 2006), relatively little is known about how recurrent excitation between pyramidal cells is involved in the ␥ rhythm, although such excitatory reverberation is thought to underlie sustained activity. We found that, if there is phasic modulation in the excitatory conductance in an RS cell, it has a significant impact on the spike timing of the cell, which is very difficult to cancel out by phasic modulation in the inhibition.…”

Gamma and beta neural activity evoked during a sensory gating paradigm: Effects of auditory, somatosensory and cross-modal stimulation

“…The outcome of these and other investigations led to the hypotheses that event-related neural activity in the gamma band reflects obligatory processing of sensory stimulus features (Clementz and Blumenfeld, 2001;Karakas and Basar, 1998), and the subsequent beta activity "flags" a stimulus as salient (Traub et al, 1999) and thus a candidate for subsequent involuntary attention switching (Whittington et al, 1997). Further supporting evidence includes the finding that gamma oscillations are generally localized to specific sensory cortical regions (Barth and MacDonald, 1996;Pantev et al, 1991;Pantev, 1995) whereas beta activity exhibits more widespread expression across cortex and more robust synchronization between cortical regions including association areas (Roelfsema et al, 1997;von Stein et al, 1999).…”