Abstract
BackgroundThe functional heterogeneity of the hippocampus along its longitudinal axis at the level of behavior is an established concept; however, the neurobiological mechanisms are still unknown. Diversifications in the functioning of intrinsic hippocampal circuitry including short-term dynamics of synaptic inputs and neuronal output, that are important determinants of information processing in the brain, may profoundly contribute to functional specializations along the hippocampus. The objectives of the present study were the examination of the role of the GABAA receptor-mediated inhibition, the μ-opioid receptors and the effect of stimulation intensity on the dynamics of both synaptic input and neuronal output of CA1 region in the dorsal and ventral hippocampus. We used recordings of field potentials from adult rat hippocampal slices evoked by brief repetitive activation of Schaffer collaterals.ResultsWe find that the local CA1 circuit of the dorsal hippocampus presents a remarkably increased dynamic range of frequency-dependent short-term changes in both input and output, ranging from strong facilitation to intense depression at low and high stimulation frequencies respectively. Furthermore, the input–output relationship in the dorsal CA1 circuit is profoundly influenced by frequency and time of presynaptic activation. Strikingly, the ventral hippocampus responds mostly with depression, displaying a rather monotonous input–output relationship over frequency and time. Partial blockade of GABAA receptor-mediated transmission (by 5 μM picrotoxin) profoundly influences input and output dynamics in the dorsal hippocampus but affected only the neuronal output in the ventral hippocampus. M-opioid receptors control short-term dynamics of input and output in the dorsal hippocampus but they play no role in the ventral hippocampus.ConclusionThe results demonstrate that information processing by CA1 local network is highly diversified between the dorsal and ventral hippocampus. Transient detection of incoming patterns of activity and frequency-dependent sustained signaling of amplified neuronal information may be assigned to the ventral and dorsal hippocampal circuitry respectively. This disparity should have profound implications for the functional roles ascribed to distinct segments along the long axis of the hippocampus.
Highlights
The functional heterogeneity of the hippocampus along its longitudinal axis at the level of behavior is an established concept; the neurobiological mechanisms are still unknown
The three stimulation intensities that produced three different levels of local network activation will be thereafter called subthreshold, suprathreshold and submaximal, respectively. We applied this experimental protocol in dorsal hippocampus (DH) and ventral hippocampus (VH) slices obtained from six rats
This study demonstrates that the CA1 circuitry of the DH displays a higher dynamic range of short-term plasticity of synaptic input and neuronal output mainly in virtue of the high scores of signal facilitation
Summary
The functional heterogeneity of the hippocampus along its longitudinal axis at the level of behavior is an established concept; the neurobiological mechanisms are still unknown. The neural network of hippocampus displays a wide range of dynamic changes in its activity and performs a variety of functions by engaging different modes of activity [9, 10]. To some extent, this is expressed by the existence of different semi-independent nodes of neural information processing along a canonical excitatory trisynaptic circuit that defines the transverse “lamellar” organization of the hippocampus [11] and is composed by the dentate gyrus and the CA3 and CA1 fields that have their own properties and perform distinct operations [12, 13]. The many functions to which hippocampus plays important roles [14,15,16,17] may impose additional demands concerning the variety of neural computations of hippocampus needed to support these functions
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