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Basolateral amygdala oscillations enable fear learning in a biophysical model.

ABSTRACT: The basolateral amygdala (BLA) is a key site where fear learning takes place through synaptic plasticity. Rodent research shows prominent low theta (∼3-6 Hz), high theta (∼6-12 Hz), and gamma (>30 Hz) rhythms in the BLA local field potential recordings. However, it is not understood what role these rhythms play in supporting the plasticity. Here, we create a biophysically detailed model of the BLA circuit to show that several classes of interneurons (PV+, SOM+, and VIP+) in the BLA can be critically involved in producing the rhythms; these rhythms promote the formation of a dedicated fear circuit shaped through rhythmic gating of spike-timing-dependent plasticity. Each class of interneurons is necessary for the plasticity. We find that the low theta rhythm is a biomarker of successful fear conditioning. Finally, we discuss how the peptide released by the VIP+ cell may alter the dynamics of plasticity to support the necessary fine timing.

SUBMITTER: Cattani A

PROVIDER: S-EPMC10168360 | biostudies-literature | 2023 May

REPOSITORIES: biostudies-literature

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Basolateral amygdala oscillations enable fear learning in a biophysical model.

Cattani Anna A Arnold Don B DB McCarthy Michelle M Kopell Nancy N

bioRxiv : the preprint server for biology 20241004

The basolateral amygdala (BLA) is a key site where fear learning takes place through synaptic plasticity. Rodent research shows prominent low theta (~3-6 Hz), high theta (~6-12 Hz), and gamma (>30 Hz) rhythms in the BLA local field potential recordings. However, it is not understood what role these rhythms play in supporting the plasticity. Here, we create a biophysically detailed model of the BLA circuit to show that several classes of interneurons (PV, SOM, and VIP) in the BLA can be criticall ...[more]

PMID: 37163011

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Project description:Here we tested a hypothesis that epileptogenesis influences expression pattern of genes in the basolateral amygdala that are critical for fear conditioning. Whole genome molecular profiling of basolateral rat amygdala was performed to compare the transcriptome changes underlying fear learning in epileptogenic and control animals. Our analysis revealed that after acquisition of fear conditioning 26 genes were regulated differently in the basolateral amygdala of both groups. Thus, our study provides the first evidence that not only the damage to the neuronal pathways but also altered composition or activity level of molecular machinery responsible for formation of emotional memories within surviving pathways can contribute to impairment in emotional learning in epileptogenic animals. Understanding the function of those genes in emotional learning provides an attractive avenue for identification of novel drug targets for treatment of emotional disorders after epileptogenesis-inducing insult. Experiment Overall Design: Experiment description: Experiment Overall Design: Array: Rat Genome 230-2.0 (Affymetrix). Experiment Overall Design: Samples: 2 biological replicates from 4 experimental groups (control unpaired = CU, CU1, control paired = CP, CP1, epileptogenic unpaired = EU, EU1, epileptogenic paired = EP, EP1). Experiment Overall Design: Animals&model: Amygdala stimulation model (Nissinen et al., 2000): Experiment Overall Design: control (C) animals = operated, not stimulated; Experiment Overall Design: epileptogenic (E) animals = stimulated, responded with "good" status epilepticus (at least 40HAFDs within first 3h of SE), not expressing spontaneous seizures through the whole study. Experiment Overall Design: All animals received 5 habituation session to the fear conditioning apparatus lasting 10 min, starting on day 5 (2 sessions on day 5 and 6 and 1 session on day 7) after stimulation (induction of SE). Experiment Overall Design: On 8th day after stimulation: Experiment Overall Design: unpaired (U) = twice received: 2min in apparatus â footshock (1.5mA, 1s)â tone (75dB for 20 sec) Experiment Overall Design: paired (P) = twice received: 2min in apparatus â tone (75dB for 20 sec) co-terminated by footshock (1.5mA, 1s). Experiment Overall Design: RNA isolation: decapitation â ipsilateral temporal lobe isolated, embed in OCT and frozen in -70C. Cut into 10Âµm sections, thionin stained (Ambion protocol), basal and lateral nuclei of the amygdala laser-microdissected; total cellular RNA isolated with PicoPure RNA isolation kit (Arcturus). Experiment Overall Design: RNA amplification: 30ng of of total cellular RNA from each rat underwent of 2 rounds of amplification using MessageAmp II aRNA kit (Ambion), according to manufacturer protocol (in vitro transcription time 14h in both rounds). Experiment Overall Design: Sample pooling: aRNA from 2 animals was pooled (10Âµg in total = 2x5Âµg) and 8 samples were labeled and hybridized: CP, CP1, CU, CU1, EP, EP1, EU, EU1; (altogether aRNA from 16 rats was used).

Dataset Information

Basolateral amygdala oscillations enable fear learning in a biophysical model.

Publications

Basolateral amygdala oscillations enable fear learning in a biophysical model.

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