Similar inhibitory processes dominate the responses of cat lateral amygdaloid projection neurons to their various afferents

To investigate the impact of inhibitory processes on responses of lateral amygdaloid (LAT) neurons, intracellular recordings were obtained from identified LAT projection neurons in barbiturate-anesthetized cats. Synaptic responses evoked by perirhinal (PRH), entorhinal (ENT), basomedial, and LAT stimulation were investigated. Regardless of stimulation site, responses consisted of an excitatory postsynaptic potential (EPSP) that either preceded and was truncated by an inhibitory postsynaptic potential (IPSP) or occurred just after the IPSP onset. IPSPs were monophasic, lasted hundreds of milliseconds, and were of such large amplitude and rapid onset that they effectively opposed the EPSPs, generally preventing orthodromic spikes. All sites elicited IPSPs with relatively negative reversal potentials around -85 mV. Experiments analyzing the underlying ionic mechanisms are presented in the companion paper. Evoked responses were similar to synaptic potentials associated with spontaneous EEG events, known as simple (small, monophasic) and complex (large, triphasic) ENT sharp potentials (SPs), with no difference between the reversals of evoked and SP-related IPSPs (-83.2 +/- 2.7 mV). IPSPs coinciding with complex SPs truncated SP-related EPSPs more rapidly and had larger amplitudes and longer durations than those related to simple SPs. These differences reflected the fact that the amplitude and duration of SP-related IPSPs were correlated with SP amplitude. Similar variations were reproduced in evoked IPSPs by varying the stimulus intensity. Low intensities generated predominantly excitatory responses consisting of EPSPs sometimes followed by small IPSPs, whereas high intensities evoked predominantly inhibitory responses comprised of a large IPSP that truncated or occluded the EPSPs. Orthodromic spikes were elicited only in a narrow range of intermediate intensities. These changes in the evoked response primarily reflected increases in the IPSP evoked at high intensities. PRH stimulation at different rostro-caudal levels demonstrated that rostral sites elicited larger EPSPs and IPSPs with shorter latencies and longer durations than caudal sites. These differences probably reflect contrasting patterns of activity spread through the PRH cortex, suggesting that the intact cortical circuitry allowed a temporally distributed activation of inhibitory interneurons and thereby partly explains the long duration and monophasic nature of the IPSPs. Inhibition, thus, plays a primary role in shaping LAT neuronal responses. The profuse intrinsic connectivity of the LAT nucleus and parahippocampal cortices may underlie the relatively invariant response pattern of LAT neurons and suggests a common mode of information processing, based upon quantitative, rather than qualitative, differences in activation of LAT circuitry. Therefore we propose that effective transmission of signals through the LAT nucleus may require activation of specifically sized neuronal ensembles, rather than widespread afferent excitation.