Abstract
The hippocampus has been thought to process auditory information. However, the properties, pathway, and role of hippocampal auditory responses are unclear. With loose-patch recordings, we found that hippocampal neurons are mainly responsive to noise and are not tonotopically organized. Their latencies are shorter than those of primary auditory cortical (A1) neurons but longer than those of medial septal (MS) neurons, suggesting that hippocampal auditory information comes from MS neurons rather than from A1 neurons. Silencing the MS blocks both hippocampal auditory responses and memory of auditory fear conditioning trained with noise and tone. Auditory fear conditioning was associated with some cues but not with a specific frequency of sound, as demonstrated by animals trained with noise, 2.5-, 5-, 10-, 15-, or 30-kHz tones, and tested with these sounds. Therefore, the noise responses of hippocampal neurons have identified a population of neurons that can be associated with auditory fear conditioning.
Highlights
The hippocampus plays a critical role in learning and memory
We found that hippocampal neurons activated by the medial septal (MS) respond only to noise stimuli in awake subjects and the noise responses of hippocampal neurons have identified a population of neurons that can be associated with behavior, which is independent of the frequency of conditioned sound
We explored the auditory response properties of hippocampal neurons, the auditory pathway to the hippocampus, and the role of hippocampal auditory responses in auditory fear conditioning using electrophysiological and behavioral assays combined with pharmacological manipulations
Summary
The hippocampus plays a critical role in learning and memory. Many behavioral experiments have been designed using sound as a cue to explore the functions of the hippocampus, such as sound discrimination (Vinogradova, 1975; O’Keefe and Nadel, 1978; Sakurai, 2002; Itskov et al, 2012; Vinnik et al, 2012), auditory recognition (Vinogradova, 1975; O’Keefe and Nadel, 1978; Sakurai, 1990) and auditory fear conditioning (O’Keefe and Nadel, 1978; LeDoux, 2000; Moita et al, 2003; Buccafusco, 2009). In the studies of the hippocampus, various sounds, such as tone bursts (Sacchetti et al, 1999; Maren and Holt, 2004; Czerniawski et al, 2012; Robinson and Bucci, 2012; Donzis et al, 2013; Kaifosh et al, 2013), clicks (O’Keefe and Nadel, 1978; McHugh et al, 2013) and noise bursts (Moita et al, 2003, 2004; Kaifosh et al, 2013) have been used as CS for auditory fear conditioning It is unclear whether hippocampal neurons respond to the sounds used as CS, where the auditory information processed by these neurons comes from, and how their sound responses are related to behavioral responses, such as freezing
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