Postnatal development of electrophysiological properties of principal neurons in the rat basolateral amygdala

Ehrlich, D. E.; Ryan, S. J.; Rainnie, D. G.

doi:10.1113/jphysiol.2012.237453

Cited by 86Neuroscience and Neuropharmacology ResearchMemory and Neural MechanismsNeural dynamics and brain function

Postnatal development of electrophysiological properties of principal neurons in the rat basolateral amygdala

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Ehrlich, D. E., Ryan, S. J., Rainnie, D. G.·2012·The Journal of Physiology

DOI 10.1113/jphysiol.2012.237453PMC PMC3487039

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Abstract

Key points The amygdala mediates emotional processing, in particular fear learning, and disruption of its function is thought to contribute to the developmental origins of psychiatric disorders like depression, anxiety and autism spectrum disorders. It is difficult to identify the causes of these disorders or provide effective intervention because most of what is known of amygdala physiology is based on the adult. Using the whole‐cell patch clamp technique, we show that neurons in the developing rat amygdala undergo drastic changes to their electrophysiology, including passive membrane properties, intrinsic currents and resonance. This provides the first evidence that amygdala neuron physiology is dynamic before adulthood, and likely to contribute to emotional development. The results help us better understand the normative development of emotional processing and identify critical periods of maturation that may be sensitive to insult. Abstract The basolateral amygdala (BLA) is critically involved in the pathophysiology of psychiatric disorders, which often emerge during brain development. Several studies have characterized postnatal changes to the morphology and biochemistry of BLA neurons, and many more have identified sensitive periods of emotional maturation. However, it is impossible to determine how BLA development contributes to emotional development or the aetiology of psychiatric disorders because no study has characterized the physiological maturation of BLA neurons. We addressed this critical knowledge gap for the first time using whole‐cell patch clamp recording in rat BLA principal neurons to measure electrophysiological properties at postnatal day (P)7, P10, P14, P21, P28 and after P35. We show that intrinsic properties of these neurons undergo significant transitions before P21 and reach maturity around P28. Specifically, we observed significant reductions in input resistance and membrane time constant of nearly 10‐ and 4‐fold, respectively, from P7 to P28. The frequency selectivity of these neurons to input also changed significantly, with peak resonance frequency increasing from 1.0 Hz at P7 to 5.7 Hz at P28. In the same period, maximal firing frequency significantly increased and doublets and triplets of action potentials emerged. Concomitantly, individual action potentials became significantly faster, firing threshold hyperpolarized 6.7 mV, the medium AHP became faster and shallower, and a fast AHP emerged. These results demonstrate neurons of the BLA undergo vast change throughout postnatal development, and studies of emotional development and treatments for juvenile psychiatric disorders should consider the dynamic physiology of the immature BLA.

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Early life may be a period of rapid change and heightened vulnerability of the amygdala to environmental influence, as well as multiple interconnected brain regions, including the hippocampus and PFC.
“This suggests that early life may be a period of rapid change and, likewise, heightened vulnerability of the amygdala to environmental influence, as well as multiple interconnected brain regions, including the hippocampus and PFC (Ehrlich and Josselyn, 2016, Ehrlich et al., 2012, Lupien et al., 2009).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Ehrlich et al., 2012

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Research works printed but not linked: 3

Ehrlich DE, Ryan SJ, Hazra R, Guo JD, Rainnie DG. 2010 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience; 2010. Postnatal development of I(h) subunit expression contributes to maturation of intrinsic resonance properties in principal neurons of the basolateral amygdala. Programme No. 885.3. [Google Scholar]
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Madsen TE, Rainnie DG. 2009 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience; 2009. Local field potentials in the rat basolateral amygdala and medial prefrontal cortex show coherent oscillations in multiple frequency bands during fear. Programme No. 132.4. [Google Scholar]

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Self-citation

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Authors: Ehrlich, D. E., Ryan, S. J., & Rainnie, D. G.
Affiliations: Emory University (US)
Corresponding author: Rainnie, D. G.
ORCID: Ehrlich, D. E.
Ryan, S. J.
Rainnie, D. G.
Venue: The Journal of Physiology
Publisher: Wiley
Published: 2012-09-03
Volume: 590
Issue: 19
Pages: 4819-4838
ISSN: 0022-3751 (ISSN-L)
1469-7793
DOI: 10.1113/jphysiol.2012.237453
PMC: PMC3487039
OpenAlex: W1481379109
Cited by: 86
References: 108
Citations by year: 2026: 5 · 2025: 5 · 2024: 4 · 2023: 1 · 2022: 7 · 2021: 6 · 2020: 10 · 2019: 7 · 2018: 8 · 2017: 9 · 2016: 5 · 2015: 12 · 2014: 5 · 2013: 2
FWCI: 2.50
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The Journal of Physiology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Mental Health (R01MH069852, MH-090729, F31MH090729, MH069852)
National Institute of General Medical Sciences (T32GM008605)
National Center for Research Resources (RR-00 165, P51RR000165)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords: basolateral amygdala, principal neurons, postnatal development, neuronal maturation, electrophysiological properties, input resistance, membrane time constant, resonant frequency, action potential firing, afterhyperpolarization, emotional development, fear learning, mental illness, rats
MeSH terms: Age Factors, Amygdala, Animals, Animals, Newborn, Female, Male, Membrane Potentials, Neurons, Rats, Sprague-Dawley, Rats, In Vitro Techniques

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Postnatal development of electrophysiological properties of principal neurons in the rat basolateral amygdala

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