Background
Adolescence is considered a critical time of life for emotional development in humans.
During this period the amygdala, which regulates emotions, undergoes structural reorganization.
Auditory fear conditioning, a form of amygdala-dependent emotional learning, occurs
differently in juvenile and adult rodents. Because this learning is mediated by plastic
changes in the thalamic and cortical inputs to lateral amygdala (LA), we investigated
changes in synaptic properties of these inputs during juvenile-to-adult transition.
Methods
Whole-cell patch clamp recording in amygdala slices from juvenile and young adult
mice was conducted to investigate long-term potentiation and basal synaptic transmission
in the thalamic and cortical inputs to LA.
Results
We show that physiological differences develop between thalamic and cortical afferents
to LA during the juvenile-to-adult transition. Although in juvenile mice the two pathways
have similar properties, in young adult mice the thalamic pathway has reduced plasticity,
increased number of quanta released by a single action potential, and decreased proportion
of silent synapses.
Conclusions
Changes in thalamic but not cortical inputs to amygdala take place during late development
and might contribute to differences in auditory fear conditioning between juveniles
and adults.
Key Words
To read this article in full you will need to make a payment
Purchase one-time access:
Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online accessOne-time access price info
- For academic or personal research use, select 'Academic and Personal'
- For corporate R&D use, select 'Corporate R&D Professionals'
Subscribe:
Subscribe to Biological PsychiatryAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- Cognitive and affective development in adolescence.Trends Cogn Sci. 2005; 9: 69-74
- The adolescent brain and age-related behavioral manifestations.Neurosci Biobehav Rev. 2000; 24: 417-463
- The amygdala and emotion: A view through fear.in: Aggleton J. The Amygdala. Oxford University Press, Oxford2000: 289-310
- Brain mechanisms of emotion and emotional learning.Curr Opin Neurobiol. 1992; 2: 191-197
- Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala.Neuron. 1999; 23: 229-232
- The amygdala: Vigilance and emotion.Mol Psychiatry. 2001; 6: 13-34
- Sexual dimorphism of the developing human brain.Prog Neuropsychopharmacol Biol Psychiatry. 1997; 21: 1185-1201
- The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages.J Neurosci. 2004; 24: 6392-6401
- Amygdalocortical sprouting continues into early adulthood: Implications for the development of normal and abnormal function during adolescence.J Comp Neurol. 2002; 453: 116-130
- Increasing interaction of amygdalar afferents with GABAergic interneurons between birth and adulthood.Cereb Cortex. 2008; 18: 1529-1535
- Ontogeny of fear-, anxiety- and depression-related behavior across adolescence in C57BL/6J mice.Behav Brain Res. 2007; 176: 210-215
- Enhanced generalization of auditory conditioned fear in juvenile mice.Learn Mem. 2009; 16: 187-192
- Equipotentiality of thalamo-amygdala and thalamo-cortico-amygdala circuits in auditory fear conditioning.J Neurosci. 1992; 12: 4501-4509
- Organization of projections to the lateral amygdala from auditory and visual areas of the thalamus in the rat.J Comp Neurol. 1999; 412: 383-409
- Fear conditioning induces a lasting potentiation of synaptic currents in vitro.Nature. 1997; 390: 607-611
- Fear conditioning induces associative long-term potentiation in the amygdala.Nature. 1997; 390: 604-607
- Fear conditioning occludes LTP-induced presynaptic enhancement of synaptic transmission in the cortical pathway to the lateral amygdala.Neuron. 2002; 34: 289-300
- Developmental emergence of fear learning corresponds with changes in amygdala synaptic plasticity.Brain Res. 2008; 1200: 58-65
- Distinct populations of NMDA receptors at subcortical and cortical inputs to principal cells of the lateral amygdala.J Neurophysiol. 1999; 81: 930-934
- Dendritic spine heterogeneity determines afferent-specific Hebbian plasticity in the amygdala.Neuron. 2005; 45: 119-131
- A pathway-specific function for different AMPA receptor subunits in amygdala long-term potentiation and fear conditioning.J Neurosci. 2007; 27: 10947-10956
- Spatiotemporal asymmetry of associative synaptic plasticity in fear conditioning pathways.Neuron. 2006; 52: 883-896
- Enhanced cortico-amygdala efficacy and suppressed fear in absence of Rap1.J Neurosci. 2008; 28: 2089-2098
- Selective gating of glutamatergic inputs to excitatory neurons of amygdala by presynaptic GABAB receptor.Neuron. 2009; 61: 917-929
- The probability of transmitter release at a mammalian central synapse.Nature. 1993; 366: 569-572
- Generation of silent synapses by acute in vivo expression of CaMKIV and CREB.Neuron. 2005; 45: 741-752
- Amplitude fluctuations of dual-component EPSCs in hippocampal pyramidal cells: Implications for long-term potentiation.Neuron. 1994; 12: 1111-1120
- Rate, timing, and cooperativity jointly determine cortical synaptic plasticity.Neuron. 2001; 32: 1149-1164
- Regulation of hippocampal transmitter release during development and long-term potentiation.Science. 1995; 269: 1730-1734
- Developmental remodeling of the retinogeniculate synapse.Neuron. 2000; 28: 955-966
- Remodeling the plasticity debate: The presynaptic locus revisited.Physiology (Bethesda). 2006; 21: 346-351
- Nonuniform probability of glutamate release at a hippocampal synapse.Science. 1993; 262: 754-757
- Changes in reliability of synaptic function as a mechanism for plasticity.Nature. 1994; 371: 704-707
- Heterogeneity of release probability, facilitation, and depletion at central synapses.Neuron. 1997; 18: 995-1008
- Efficacy of thalamocortical and intracortical synaptic connections: Quanta, innervation, and reliability.Neuron. 1999; 23: 385-397
- Synaptic plasticity at thalamocortical synapses in developing rat somatosensory cortex: LTP, LTD, and silent synapses.J Neurobiol. 1999; 41: 92-101
- Silent synapses during development of thalamocortical inputs.Neuron. 1997; 18: 269-280
- Extrasynaptic glutamate spillover in the hippocampus: Dependence on temperature and the role of active glutamate uptake.Neuron. 1997; 18: 281-293
- Glutamate uptake determines pathway specificity of long-term potentiation in the neural circuitry of fear conditioning.Neuron. 2004; 41: 139-151
- Direct measurement of somatic voltage clamp errors in central neurons.Nat Neurosci. 2008; 11: 790-798
- L-type voltage-gated calcium channels mediate NMDA-independent associative long-term potentiation at thalamic input synapses to the amygdala.J Neurosci. 1999; 19: 10512-10519
- Chronic nicotine exposure induces a long-lasting and pathway-specific facilitation of LTP in the amygdala.Learn Mem. 2008; 15: 603-610
- A million dollar question: Does LTP = memory?.Neuron. 1998; 20: 1-2
- Stathmin, a gene enriched in the amygdala, controls both learned and innate fear.Cell. 2005; 123: 697-709
- Long-term potentiation in freely moving rats reveals asymmetries in thalamic and cortical inputs to the lateral amygdala.Eur J Neurosci. 2003; 17: 2703-2715
- Temporary inactivation of the perirhinal cortex by muscimol injections block acquisition and expression of fear-potentiated startle.Eur J Neurosci. 2004; 19: 713-720
- Involvement of subcortical and cortical afferents to the lateral nucleus of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli.J Neurosci. 1995; 15: 2312-2327
- A thalamo-cortico-amygdala pathway mediates auditory fear conditioning in the intact brain.Eur J Neurosci. 2006; 24: 894-900
Article info
Publication history
Published online: August 25, 2009
Accepted:
July 7,
2009
Received in revised form:
July 6,
2009
Received:
March 20,
2009
Identification
Copyright
© 2009 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.
