High frequency (200 Hz) oscillations and firing patterns in the basolateral amygdala and dorsal endopiriform nucleus of the behaving rat

The known repertoire of rhythms in the amygdala and paleocortex includes a range of oscillations from slow waves (<1 Hz) to fast gamma (40-100 Hz). In the present report, we show approximately 200 Hz oscillations in the basolateral nucleus of the amygdala (BL) and the adjacent dorsal endopiriform nucleus (EPN) of the behaving rat. Microwire techniques were applied for recording single units and field activity from these structures and EEG from the dorsal or temporal CA1 subfields of the hippocampus. Units from both EPN and BL exhibited similar irregular firing patterns with bursts. The mean firing rates in EPN were <1 Hz, whereas units in the BL fired in a range of <1-17 Hz. Neuronal activity in both BL and EPN was phase-locked with high-frequency field oscillations (HFO, approximately 200 Hz). Amygdaloid/EPN HFO displayed on average lower numbers of cycles and smaller amplitudes than hippocampal ripples. Neuronal firing and HFO in the BL and EPN were state dependent with a maximal occurrence during slow-wave sleep (SWS), being lower during waking and paradoxical sleep. Cross-correlation between hippocampal ripples and EPN or BL units and field HFO did not reveal any synchrony. These data suggest common principles of temporal coding in BL and EPN in certain behavioural states via short scale population synchrony though they convey signals of different modalities.

[1]  Constantine Pavlides,et al.  Single-unit activity in the lateral nucleus of the amygdala and overlying areas of the striatum in freely behaving rats: rates, discharge patterns, and responses to acoustic stimuli. , 1993, Behavioral neuroscience.

[2]  M. Washburn,et al.  Electrophysiological and morphological properties of rat basolateral amygdaloid neurons in vitro , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  M B Jackson,et al.  Voltage imaging of epileptiform activity in slices from rat piriform cortex: onset and propagation. , 1998, Journal of neurophysiology.

[4]  Kindling-induced epileptiform potentials in piriform cortex slices originate in the underlying endopiriform nucleus. , 1996, Journal of neurophysiology.

[5]  T. Robbins,et al.  The basolateral amygdala-ventral striatal system and conditioned place preference: Further evidence of limbic-striatal interactions underlying reward-related processes , 1991, Neuroscience.

[6]  G Buzsáki,et al.  Memory consolidation during sleep: a neurophysiological perspective. , 1998, Journal of sleep research.

[7]  G. Buzsáki,et al.  High-Frequency Oscillations in the Output Networks of the Hippocampal–Entorhinal Axis of the Freely Behaving Rat , 1996, The Journal of Neuroscience.

[8]  D. Paré,et al.  Projection Cells and Interneurons of the Lateral and Basolateral Amygdala: Distinct Firing Patterns and Differential Relation to Theta and Delta Rhythms in Conscious Cats , 1996, The Journal of Neuroscience.

[9]  A. Bragin,et al.  Chronic Epileptogenesis Requires Development of a Network of Pathologically Interconnected Neuron Clusters: A Hypothesis , 2000, Epilepsia.

[10]  WH Hoffman,et al.  Bursting-induced epileptiform EPSPs in slices of piriform cortex are generated by deep cells , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  G. Buzsáki,et al.  Long-term potentiation induced by physiologically relevant stimulus patterns , 1987, Brain Research.

[12]  A. Grace,et al.  Dopamine Attenuates Prefrontal Cortical Suppression of Sensory Inputs to the Basolateral Amygdala of Rats , 2001, The Journal of Neuroscience.

[13]  T. van Groen,et al.  Extrinsic projections from area CA1 of the rat hippocampus: Olfactory, cortical, subcortical, and bilateral hippocampal formation projections , 1990, The Journal of comparative neurology.

[14]  G. Buzsáki,et al.  Cellular bases of hippocampal EEG in the behaving rat , 1983, Brain Research Reviews.

[15]  Charles L. Wilson,et al.  Hippocampal and Entorhinal Cortex High‐Frequency Oscillations (100–500 Hz) in Human Epileptic Brain and in Kainic Acid‐Treated Rats with Chronic Seizures , 1999, Epilepsia.

[16]  D. Paré,et al.  Bursting and oscillating neurons of the cat basolateral amygdaloid complex in vivo: electrophysiological properties and morphological features. , 1995, Journal of neurophysiology.

[17]  H. Pape,et al.  Putative Cortical and Thalamic Inputs Elicit Convergent Excitation in a Population of GABAergic Interneurons of the Lateral Amygdala , 2000, The Journal of Neuroscience.

[18]  Charles L. Wilson,et al.  High‐frequency oscillations in human brain , 1999, Hippocampus.

[19]  B. McNaughton,et al.  Reactivation of Hippocampal Cell Assemblies: Effects of Behavioral State, Experience, and EEG Dynamics , 1999, The Journal of Neuroscience.

[20]  L. Haberly,et al.  Intrinsic and efferent connections of the endopiriform nucleus in rat , 1999, The Journal of comparative neurology.

[21]  D. Paré,et al.  Amygdalo-entorhinal relations and their reflection in the hippocampal formation: generation of sharp sleep potentials , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  L. Haberly,et al.  Deep neurons in piriform cortex. I. Morphology and synaptically evoked responses including a unique high-amplitude paired shock facilitation. , 1989, Journal of neurophysiology.

[23]  D. Paré,et al.  Spontaneous activity of the perirhinal cortex in behaving cats , 1999, Neuroscience.

[24]  E. Asprodini,et al.  Intracellular recordings from morphologically identified neurons of the basolateral amygdala. , 1993, Journal of neurophysiology.

[25]  M. Wilson,et al.  Coordinated Interactions between Hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep , 1998, Neuron.

[26]  G. Buzsáki,et al.  Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  M. Jouvet,et al.  Hypothalamo‐preoptic Histaminergic Projections in Sleep‐Wake Control in the Cat , 1994, The European journal of neuroscience.

[28]  G. Buzsáki,et al.  High-frequency network oscillation in the hippocampus. , 1992, Science.

[29]  Dawn R. Collins,et al.  Amygdala oscillations and the consolidation of emotional memories , 2002, Trends in Cognitive Sciences.

[30]  L. Swanson,et al.  What is the amygdala? , 1998, Trends in Neurosciences.

[31]  Denis Paré,et al.  The electrophysiology of the olfactory–hippocampal circuit in the isolated and perfused adult mammalian brain in vitro , 1991, Hippocampus.

[32]  Charles L. Wilson,et al.  Local Generation of Fast Ripples in Epileptic Brain , 2002, The Journal of Neuroscience.

[33]  G Buzsáki,et al.  The hippocampo-neocortical dialogue. , 1996, Cerebral cortex.

[34]  G. Buzsáki Hippocampal sharp waves: Their origin and significance , 1986, Brain Research.

[35]  D. Paré,et al.  Slow and fast (gamma) neuronal oscillations in the perirhinal cortex and lateral amygdala. , 2001, Journal of neurophysiology.