From anxiety to autism: spectrum of abnormal social behaviors modeled by progressive disruption of inhibitory neuronal function in the basolateral amygdala in Wistar rats
Abstract
Rationale Social behaviors are disrupted in several psychiatric disorders. The amygdala is a key brain region involved in social behaviors, and amygdala pathology has been implicated in disease states ranging from social anxiety disorder to autism.Objective To test the effects of progressive disruption of the inhibitory function within the basolateral nucleus of the amygdala (BLA) on conspecific social interaction in rats and investigate functional networks from the ventral medial prefrontal cortex (mPFCv) to the BLA.Materials and methods BLA inhibitory tone was disrupted by priming it with the stress-peptide corticotrophin releasing factor (CRF) receptor agonist urocortin 1 (Ucn 1, 6 fmol), or by selective lesioning of a subset of BLA-GABAergic interneurons containing neurokinin 1 receptors using the targeted toxin SSP-Saporin. The effects of the disruption of GABAergic tone in the BLA were examined using a repeated exposure and habituation paradigm of social interaction (SI/h). Lesions and selectivity of lesions were confirmed postmortem. Additionally, effects of stimulating mPFCv on cFos activity in interneurons of the BLA were examined.Results Rats primed with Ucn 1 showed persistent social inhibition, which could be overcome with habituation, putatively modeling social anxiety. Rats with a selective lesioning of a subset of GABAergic interneurons in the BLA exhibited persistent social inhibition that was not reversed by SI/h paradigm. We also demonstrate selective functional inputs to this subset of interneurons when mPFCv was activated.Conclusions These models with different gradations of disrupted BLA inhibition could help to study social dysfunction in disorders ranging from social anxiety to autism spectrum disorders.
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The amygdala is an important neural substrate for processing components of social information and behavior in humans and laboratory animals.
“the amygdala has been characterized as one of the important neural substrates for processing components of social information and behavior in both humans and laboratory animals”
From Rewards, aversions and affect in adolescence: emerging convergences across laboratory animal and human data (2011) · cites this paper as Truitt et al, 2007
Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Shrestha, S., & Offer, S. M. (2016) · Medical Epigenetics · doi:10.1159/000444713 · Cited by 8,949 · see citing works
Frith, C., & Frith, U. (2005) · Current Biology · doi:10.1016/j.cub.2005.08.041 · Cited by 3,494 · see citing works
The eyes have it: the neuroethology, function and evolution of social gaze
Emery, N. J. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00025-7 · Cited by 2,037 · see citing works
The rat brain in stereotaxic coordinates (2nd edn)
Herman, J. P., & Watson, S. J. (1987) · Trends in Neurosciences · doi:10.1016/0166-2236(87)90017-8 · Cited by 1,751 · see citing works
Gaze fixation and the neural circuitry of face processing in autism
Dalton, K. M., Nacewicz, B. M., Johnstone, T., Schaefer, H. S., Gernsbacher, M. A., Goldsmith, H. H., Alexander, A. L., & Davidson, R. J. (2005) · Nature Neuroscience · doi:10.1038/nn1421 · Cited by 1,543 · see citing works
The neurobiology of social cognition
Adolphs, R. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00202-6 · Cited by 1,432 · see citing works
Social intelligence in the normal and autistic brain: An fMRI study
Baron‐Cohen, S., Ring, H. A., Wheelwright, S., Bullmore, E. T., Brammer, M. J., Simmons, A., & Williams, S. C. R. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00621.x · Cited by 1,320 · see citing works
The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning
LeDoux, J., Cicchetti, P., Xagoraris, A., & Romanski, L. (1990) · The Journal of Neuroscience · doi:10.1523/jneurosci.10-04-01062.1990 · Cited by 1,167 · see citing works
Baron-Cohen, S., Ring, H. A., Bullmore, E. T., Wheelwright, S., Ashwin, C., & Williams, S. C. R. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00011-7 · Cited by 1,130 · see citing works
GABAergic Interneurons Implications for Understanding Schizophrenia and Bipolar Disorder
Benes, F. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00225-1 · Cited by 1,082 · see citing works
Social Intelligence in the Normal and Autistic Brain: An fMRI Study
Baron‐Cohen, S., RING, H. A., Wheelwright, S. J., Bullmore, E. T., Brammer, M. J., Simmons, A., & Williams, S. (2002) · The MIT Press eBooks · doi:10.7551/mitpress/3077.003.0028 · Cited by 1,044 · see citing works
Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology
Watson, R. E., Wiegand, S. J., Clough, R. W., & Hoffman, G. E. (1986) · Peptides · doi:10.1016/0196-9781(86)90076-8 · Cited by 933 · see citing works
Neuroanatomic observations of the brain in autism: a review and future directions
Bauman, M. L., & Kemper, T. L. (2005) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2004.09.006 · Cited by 919 · see citing works
New Vistas on Amygdala Networks in Conditioned Fear
Paré, D., Quirk, G. J., & Ledoux, J. E. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00153.2004 · Cited by 841 · cited 1× · see citing works
“As an alternative to the monosynaptic mPFCv BLA interneuron circuit, it has been reported that stimulation of mPFCv leads to activation in the intercalated cells, which in turn supply the inhibitory action in the amygdala of mPFCv stimulation (Berretta et al. 2005; Pare et al. 2004).”
BackgroundThe functional neuroanatomy of social behaviour
Critchley, H. D., Daly, E. M., Bullmore, E. T., Williams, S. C. R., Van Amelsvoort, T., Robertson, D. M., Rowe, A., Phillips, M., McAlonan, G., Howlin, P., et al. (2000) · Brain · doi:10.1093/brain/123.11.2203 · Cited by 816 · see citing works
Ghashghaei, H. T., & Barbas, H. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00446-3 · Cited by 785 · see citing works
Contrasting Roles of Basolateral Amygdala and Orbitofrontal Cortex in Impulsive Choice
Winstanley, C. A., Theobald, D. E. H., Cardinal, R. N., & Robbins, T. W. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5606-03.2004 · Cited by 675 · see citing works
Amygdala circuitry in attentional and representational processes.
Holland, P., & Gallagher, M. (1999) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(98)01271-6 · Cited by 613 · see citing works
Increased Amygdala Activation to Angry and Contemptuous Faces in Generalized Social Phobia
Stein, M. B., Goldin, P. R., Sareen, J., Zorrilla, L. T. E., & Brown, G. G. (2002) · Archives of General Psychiatry · doi:10.1001/archpsyc.59.11.1027 · Cited by 582 · see citing works
Schoenbaum, G., Chiba, A. A., & Gallagher, M. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-05-01876.1999 · Cited by 579 · see citing works
Impaired Recognition of Social Emotions following Amygdala Damage
Adolphs, R., Baron-Cohen, S., & Tranel, D. (2002) · Journal of Cognitive Neuroscience · doi:10.1162/089892902760807258 · Cited by 510 · see citing works
Schoenbaum, G., Setlow, B., Saddoris, M. P., & Gallagher, M. (2003) · Neuron · doi:10.1016/s0896-6273(03)00474-4 · Cited by 484 · see citing works
Neural systems involved in 'theory of mind'
Siegal, M., & Varley, R. A. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn844 · Cited by 427 · see citing works
Rosenkranz, J., & Grace, A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-01-00324.2002 · Cited by 422 · see citing works
Haznedar, M. M., Buchsbaum, M. S., Wei, T.-C., Hof, P. R., Cartwright, C., Bienstock, C. A., & Hollander, E. (2000) · American Journal of Psychiatry · doi:10.1176/appi.ajp.157.12.1994 · Cited by 420 · see citing works
Orbitofrontal cortex, associative learning and expectancies
Schoenbaum, G., & Roesch, M. (2005) · Neuron · doi:10.1016/j.neuron.2005.07.018 · Cited by 404 · see citing works
Amygdala–frontal interactions and reward expectancy
Holland, P. C., & Gallagher, M. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.03.007 · Cited by 390 · see citing works
Different Roles for Orbitofrontal Cortex and Basolateral Amygdala in a Reinforcer Devaluation Task
Pickens, C. L., Saddoris, M. P., Setlow, B., Gallagher, M., Holland, P. C., & Schoenbaum, G. M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-35-11078.2003 · Cited by 379 · see citing works
Identification of a Potential Ejaculation Generator in the Spinal Cord
Truitt, W. A., & Coolen, L. M. (2002) · Science · doi:10.1126/science.1073885 · Cited by 362 · see citing works
Self-citationAmaral, D. G. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01307-5 · Cited by 349 · see citing works
Rosenkranz, J. A., Moore, H., & Grace, A. A. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-35-11054.2003 · Cited by 344 · see citing works
Rosenkranz, J. A., & Grace, A. A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-11-04090.2001 · Cited by 334 · see citing works
Response of neurons in the macaque amygdala to complex social stimuli
Brothers, L., Ring, B., & Kling, A. S. (1990) · Behavioural Brain Research · doi:10.1016/0166-4328(90)90108-q · Cited by 321 · see citing works
Regulation of anxiety by GABAA receptors in the rat amygdala
Sanders, S., & Shekhar, A. (1995) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)00153-n · Cited by 319 · see citing works
Self-citationUnderstanding emotions from standardized facial expressions in autism and normal development
Castelli, F. (2005) · Autism · doi:10.1177/1362361305056082 · Cited by 317 · see citing works
Rainnie, D. G., Bergeron, R., Sajdyk, T. J., Patil, M. M., Gehlert, D. R., & Shekhar, A. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5740-03.2004 · Cited by 293 · see citing works
Self-citationInhibitory transmission in the basolateral amygdala
Rainnie, D. G., Asprodini, E., & Shinnick‐Gallagher, P. (1991) · Journal of Neurophysiology · doi:10.1152/jn.1991.66.3.999 · Cited by 280 · see citing works
(2004) · PubMed · Cited by 272 · see citing works
Rosenkranz, J. A., & Grace, A. A. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-24-11027.1999 · Cited by 253 · see citing works
Association of tuberous sclerosis of temporal lobes with autism and atypical autism
Bolton, P., & Griffiths, P. D. (1997) · The Lancet · doi:10.1016/s0140-6736(97)80012-8 · Cited by 250 · see citing works
Increased social fear and decreased fear of objects in monkeys with neonatal amygdala lesions
Prather, M. D., Lavenex, P., Mauldin-Jourdain, M. L., Mason, W. A., Capitanio, J. P., Mendoza, S. P., & Amaral, D. G. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00445-6 · Cited by 248 · see citing works
Role of stress, corticotrophin releasing factor (CRF) and amygdala plasticity in chronic anxiety
Shekhar, A., Truitt, W., Rainnie, D., & Sajdyk, T. (2005) · Stress · doi:10.1080/10253890500504557 · Cited by 237 · see citing works
Self-citationSchoenbaum, G. M., Chiba, A. A., & Gallagher, M. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-13-05179.2000 · Cited by 223 · see citing works
Infralimbic cortex activation increases c-fos expression in intercalated neurons of the amygdala
Berretta, S., Pantazopoulos, H., Caldera, M., Pantazopoulos, P., & Paré, D. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.01.020 · Cited by 223 · see citing works
Colocalization of calcium-binding proteins and GABA in neurons of the rat basolateral amygdala
McDonald, A. J., & Mascagni, F. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00214-7 · Cited by 221 · see citing works
Rapid Associative Encoding in Basolateral Amygdala Depends on Connections with Orbitofrontal Cortex
Saddoris, M. P., Gallagher, M., & Schoenbaum, G. M. (2005) · Neuron · doi:10.1016/j.neuron.2005.02.018 · Cited by 213 · see citing works
Wang, S.-J., Wang, K., & Wang, W.-C. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.01.019 · Cited by 210 · see citing works
Sajdyk, T. J., Schober, D. A., Gehlert, D. R., & Shekhar, A. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00132-6 · Cited by 191 · see citing works
Self-citationMascagni, F., McDonald, A. J., & Coleman, J. R. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90016-9 · Cited by 186 · see citing works
McDonald, A. J., & Betette, R. L. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00481-4 · Cited by 177 · see citing works
Regulation of conditioned responses of basolateral amygdala neurons
GRACE, A., & ROSENKRANZ, J. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00909-5 · Cited by 172 · see citing works
Is There an Amygdala and How Far Does It Extend?
McDonald, A. J. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07067.x · Cited by 169 · see citing works
Excitatory transmission in the basolateral amygdala
Rainnie, D. G., Asprodini, E., & Shinnick‐Gallagher, P. (1991) · Journal of Neurophysiology · doi:10.1152/jn.1991.66.3.986 · Cited by 165 · see citing works
Mascagni, F., & McDonald, A. J. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02625-8 · Cited by 157 · see citing works
Schneier, F. R., Blanco, C., Antia, S. X., & Liebowitz, M. R. (2002) · Psychiatric Clinics of North America · doi:10.1016/s0193-953x(02)00018-7 · Cited by 154 · see citing works
McDonald, A. J., & Mascagni, F. (2002) · Brain Research · doi:10.1016/s0006-8993(02)02650-1 · Cited by 152 · see citing works
Non‐human primate models of childhood psychopathology: the promise and the limitations
Machado, C. J., & Bachevalier, J. (2002) · Journal of Child Psychology and Psychiatry · doi:10.1111/1469-7610.00103 · Cited by 146 · see citing works
Shekhar, A. (1993) · Brain Research · doi:10.1016/0006-8993(93)90742-6 · Cited by 143 · see citing works
Self-citationVentral temporal cortex in the rat: Connections of secondary auditory areas Te2 and Te3
Arnault, P., & Roger, M. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.903020109 · Cited by 139 · see citing works
The Amygdala, Panic Disorder, and Cardiovascular Responses
Shekhar, A., Sajdyk, T. J., Gehlert, D. R., & Rainnie, D. G. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07090.x · Cited by 137 · see citing works
Self-citationPharmacological Characterisation of a Modified Social Interaction Model of Anxiety in the Rat
Guy, A. P., & Gardner, C. R. (2008) · Neuropsychobiology · doi:10.1159/000118187 · Cited by 133 · see citing works
The Neuropathology of Autism: A Review
Pickett, J., & London, E. (2005) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/01.jnen.0000186921.42592.6c · Cited by 122 · see citing works
Brinley-Reed, M., Mascagni, F., & MCDONALD, A. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(95)12212-5 · Cited by 114 · see citing works
Studies of Altered Social Cognition in Neuropsychiatric Disorders Using Functional Neuroimaging
Grady, C. L., & Keightley, M. (2002) · The Canadian Journal of Psychiatry · doi:10.1177/070674370204700403 · Cited by 112 · see citing works
Sajdyk, T. J., & Shekhar, A. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00594-5 · Cited by 107 · see citing works
Self-citationThe amygdala and related structures in the pathophysiology of autism.
Sweeten, T. L., Posey, D., Shekhar, A., & McDougle, C. (2002) · Pharmacology, Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00697-9 · Cited by 106 · see citing works
Self-citationMuller, J. F., Mascagni, F., & McDonald, A. J. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10435 · Cited by 100 · see citing works
Moncho-Bogani, J., Martínez‐Garciá, F., Novejarque, A., & Lanuza, E. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04036.x · Cited by 93 · see citing works
Social Cognition and Its Neural Correlates in Schizophrenia and Autism
Abdi, Z., & Sharma, T. (2004) · CNS Spectrums · doi:10.1017/s1092852900009317 · Cited by 91 · see citing works
Sanders, S., & Shekhar, A. (1995) · Biological Psychiatry · doi:10.1016/0006-3223(94)00183-4 · Cited by 88 · see citing works
Self-citationEarly amygdala damage in the rat as a model for neurodevelopmental psychopathological disorders
Wolterink, G., Daenen, L. E. W. P. M., Dubbeldam, S., Gerrits, M. A. F. M., van Rijn, R. S., Kruse, C. G., Heijden, J. A. M. V. D., & van Ree, J. M. (2001) · European Neuropsychopharmacology · doi:10.1016/s0924-977x(00)00138-3 · Cited by 85 · see citing works
de Lima, A. D., Merten, M. D. P., & Voigt, T. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970602)382:2 · Cited by 80 · see citing works
McDannald, M. A., Saddoris, M. P., Gallagher, M., & Holland, P. C. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.5301-04.2005 · Cited by 78 · see citing works
Brief report: Medial temporal lobe and autism: A putative animal model in primates
Bachevalier, J. (1996) · Journal of Autism and Developmental Disorders · doi:10.1007/bf02172015 · Cited by 70 · see citing works
Clinical guidelines: Dosing and switching strategies for long-acting risperidone.
Marder, S. R., Conley, R. R., Ereshefsky, L., Kane, J. M., & Turner, M. S. (2003) · PubMed · Cited by 62 · see citing works
Bauman, M. D., & Amaral, D. G. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.07.040 · Cited by 59 · see citing works
Social phobia: etiology, neurobiology, and treatment.
Coupland, N. J. (2001) · PubMed · Cited by 38 · see citing works
Younossi‐Hartenstein, A., Ehlers, U., & Hartenstein, V. (2000) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(20000124)416:4 · Cited by 33 · see citing works
Rosenkranz, J. A., & Grace, A. A. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07107.x · Cited by 30 · see citing works
Fear-potentiated startle elevates catecholamine levels in the dorsomedial hypothalamus of rats.
Shekhar, A., Katner, J., Rusche, W., Sajdyk, T., & Simon, J. (1994) · Pharmacology, Biochemistry and Behavior · doi:10.1016/0091-3057(94)90564-9 · Cited by 28 · see citing works
Self-citationSajdyk, T., Katner, J., & Shekhar, A. (1997) · Progress in Neuro-psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(96)00138-8 · Cited by 23 · see citing works
Self-citationCousens, G. A., & Otto, T. (2003) · Integrative Psychological and Behavioral Science · doi:10.1007/bf02688858 · Cited by 22 · see citing works
Subtypes of substance P receptor immunoreactive interneurons in the rat basolateral amygdala
Levita, L., Mania, I., & Rainnie, D. G. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02870-1 · Cited by 20 · see citing works
The Abnormal Regulation of Gene Expression in Autistic Brain Tissue
Purcell, A. E., Jeon, O., & Pevsner, J. (2001) · Journal of Autism and Developmental Disorders · doi:10.1023/a:1013290826504 · Cited by 19 · see citing works
Bachevalier, J., & Málková, L. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.4.989 · Cited by 19 · see citing works
Fashena, D. (1999) · doi:10.1002/(sici)1096-9861(19990412)406:3
Flagged first, then by citations
Cited by
Sorted by citations
Bilbo, S. D., Block, C. L., Bolton, J. L., Hanamsagar, R., & Tran, P. K. (2017) · Experimental Neurology · doi:10.1016/j.expneurol.2017.07.002 · Cited by 323 · see citing works
Spear, L. P. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.08.001 · Cited by 292 · see citing works
Sensory, emotional and cognitive contributions to anxiety in autism spectrum disorders
South, M., & Rodgers, J. (2017) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00020 · Cited by 270 · see citing works
“To date, however, there has been little published research specifically related to the mechanisms that link mPFC, anxiety and autism symptoms (though see possible relationships in rodent models, Truitt et al., 2007).”
BackgroundBasolateral amygdala and stress-induced hyperexcitability affect motivated behaviors and addiction
Sharp, B. M. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.161 · Cited by 244 · see citing works
The basolateral amygdala γ‐aminobutyric acidergic system in health and disease
Prager, E. M., Bergstrom, H. C., Wynn, G. H., & Braga, M. F. M. (2015) · Journal of Neuroscience Research · doi:10.1002/jnr.23690 · Cited by 178 · see citing works
Social learning and amygdala disruptions in Nf1 mice are rescued by blocking p21-activated kinase
Molosh, A. I., Johnson, P. L., Spence, J. P., Arendt, D. H., Federici, L. M., Bernabe, C., Janasik, S. P., Segu, Z. M., Khanna, R., Goswami, C. P., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3822 · Cited by 137 · see citing works
Self-citationNinan, I. (2011) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07430.x · Cited by 110 · see citing works
Giesbrecht, C. J., Mackay, J. P., Silveira, H., Urban, J. H., & Colmers, W. F. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2306-10.2010 · Cited by 108 · see citing works
RDoC-based categorization of amygdala functions and its implications in autism
Hennessey, T., Andari, E., & Rainnie, D. G. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.04.007 · Cited by 105 · see citing works
Truitt, W. A., Johnson, P. L., Dietrich, A. D., Fitz, S. D., & Shekhar, A. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.01.083 · Cited by 98 · see citing works
Self-citationEhrlich, D. E., Ryan, S. J., & Rainnie, D. G. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.237453 · Cited by 86 · see citing works
Postnatal maturation of GABAergic transmission in the rat basolateral amygdala.
Ehrlich, D. E., Ryan, S., Hazra, R., Guo, J.-D., & Rainnie, D. (2013) · Journal of Neurophysiology · doi:10.1152/jn.01105.2012 · Cited by 84 · see citing works
Male predominance in autism: neuroendocrine influences on arousal and social anxiety
Pfaff, D. W., Rapin, I., & Goldman, S. (2011) · Autism Research · doi:10.1002/aur.191 · Cited by 83 · see citing works
Kalueff, A. V. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.11.011 · Cited by 66 · see citing works
Jodo, E. (2013) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2013.06.002 · Cited by 62 · see citing works
Differential serotonergic innervation of the amygdala in bonobos and chimpanzees
Stimpson, C. D., Barger, N., Taglialatela, J. P., Gendron‐Fitzpatrick, A., Hof, P. R., Hopkins, W. D., & Sherwood, C. C. (2015) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsv128 · Cited by 58 · see citing works
Early deprivation induces competitive subordinance in C57BL/6 male mice
Benner, S., Endo, T., Endo, N., Kakeyama, M., & Tohyama, C. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.06.018 · Cited by 54 · see citing works
Better fear conditioning is associated with reduced symptom severity in autism spectrum disorders
South, M., Larson, M. J., White, S. E., Dana, J., & Crowley, M. J. (2011) · Autism Research · doi:10.1002/aur.221 · Cited by 56 · see citing works
Morphology and Dendritic Maturation of Developing Principal Neurons in the Rat Basolateral Amygdala
Ryan, S., Ehrlich, D. E., & Rainnie, D. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0939-x · Cited by 52 · see citing works
Mechanisms and functional implications of social buffering in infants: Lessons from animal models
Sullivan, R. M., & Perry, R. E. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1087425 · Cited by 52 · see citing works
Mast Cells, Stress, Fear and Autism Spectrum Disorder
Theoharides, T. C., Kavalioti, M., & Tsilioni, I. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20153611 · Cited by 55 · see citing works
Prenatal VPA Exposure and Changes in Sensory Processing by the Superior Colliculus
Dendrinos, G., Hemelt, M. E., & Keller, A. (2011) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2011.00068 · Cited by 50 · see citing works
Neural correlates of MDMA (“Ecstasy”)-induced social interaction in rats
Thompson, M. R., Hunt, G. E., & McGregor, I. S. (2008) · Social Neuroscience · doi:10.1080/17470910802045042 · Cited by 48 · see citing works
Villarroel, H. S., Bompolaki, M., Mackay, J. P., Tapia, A. P. M., Michaelson, S. D., Leitermann, R. J., Marr, R. A., Urban, J. H., & Colmers, W. F. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.3528-17.2018 · Cited by 45 · see citing works
Reznikov, L. R., Reagan, L. P., & Fadel, J. R. (2008) · Brain Research · doi:10.1016/j.brainres.2008.12.022 · Cited by 43 · see citing works
Zhang, W., & Rosenkranz, J. A. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.33 · Cited by 41 · see citing works
Injured brain regions associated with anxiety in Vietnam veterans
Knutson, K. M., Rakowsky, S. T., Solomon, J. M., Krüeger, F., Raymont, V., Tierney, M. C., Wassermann, E. M., & Grafman, J. H. (2013) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2013.01.003 · Cited by 39 · see citing works
The Role of the Medial Prefrontal Cortex in Regulating Social Familiarity-Induced Anxiolysis
Lungwitz, E. A., Stuber, G. D., Johnson, P. L., Dietrich, A. D., Schartz, N. D., Hanrahan, B., Shekhar, A., & Truitt, W. A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.302 · Cited by 39 · see citing works
Self-citationAutism and EMF? Plausibility of a pathophysiological link – Part I
Herbert, M. R., & Sage, C. (2013) · Pathophysiology · doi:10.1016/j.pathophys.2013.08.001 · Cited by 35 · see citing works
Séguin, D., Pac, S., Wang, J., Nicolson, R., Martínez-Trujillo, J., & Duerden, E. G. (2021) · Brain and Behavior · doi:10.1002/brb3.2299 · Cited by 37 · see citing works
Katayama, T., Jodo, E., Suzuki, Y., Hoshino, K.-Y., Takeuchi, S., & Kayama, Y. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.01.002 · Cited by 32 · see citing works
Ferrara, N. C., Trask, S., & Rosenkranz, J. (2021) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.01.021 · Cited by 26 · see citing works
Traumatic Stress Produces Delayed Alterations of Synaptic Plasticity in Basolateral Amygdala
Zhang, H., Meng, S., Guo, X., Zhang, J., Zhang, W., Chen, Y., Lü, L., Yang, J., & Xue, Y.-X. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.02394 · Cited by 29 · see citing works
Jodo, E., Katayama, T., Okamoto, M., Suzuki, Y., Hoshino, K.-Y., & Kayama, Y. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.08.017 · Cited by 27 · see citing works
Xu, L., Zheng, X., Yao, S., Li, J., Fu, M., Li, K., Zhao, W., Li, H., Becker, B., & Kendrick, K. M. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119010 · Cited by 27 · see citing works
Autism and EMF? Plausibility of a pathophysiological link part II
Herbert, M. R., & Sage, C. (2013) · Pathophysiology · doi:10.1016/j.pathophys.2013.08.002 · Cited by 27 · see citing works
Varlinskaya, E. I., SPEAR, L. P., & Diaz, M. R. (2018) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.09.003 · Cited by 23 · see citing works
Rostkowski, A. B., Leitermann, R. J., & Urban, J. H. (2013) · Neuropeptides · doi:10.1016/j.npep.2012.12.004 · Cited by 23 · see citing works
Knight, C. P., Hauser, S. R., Waeiss, R. A., Molosh, A. I., Johnson, P. L., Truitt, W. A., McBride, W. J., Bell, R. L., Shekhar, A., & Rodd, Z. A. (2020) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.119.262097 · Cited by 25 · see citing works
Self-citationDevelopmental Shifts in Amygdala Activity during a High Social Drive State
Ferrara, N. C., Trask, S., Avonts, B., Loh, M. K., Padival, M., & Rosenkranz, J. A. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1414-21.2021 · Cited by 22 · see citing works
Zahedi, E., Sadr, S. S., Sanaeierad, A., & Roghani, M. (2023) · Metabolic Brain Disease · doi:10.1007/s11011-023-01227-1 · Cited by 21 · see citing works
Sreepathi, H. K., & Ferraguti, F. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.12.006 · Cited by 21 · see citing works
Amygdala volume and social anxiety symptom severity: Does segmentation technique matter?
Jayakar, R., Tone, E. B., Crosson, B., Turner, J. A., Anderson, P. L., Phan, K. L., & Klumpp, H. (2019) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2019.111006 · Cited by 20 · see citing works
Hennessy, A., Séguin, D., Correa, S., Wang, J., Martínez-Trujillo, J., Nicolson, R., & Duerden, E. G. (2022) · Autism · doi:10.1177/13623613221127512 · Cited by 20 · see citing works
Environmental insults in early life and submissiveness later in life in mouse models
Benner, S., Endo, T., Kakeyama, M., & Tohyama, C. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00091 · Cited by 19 · see citing works
Ancheta, L. R., Shramm, P. A., Bouajram, R., Higgins, D., & Lappi, D. A. (2022) · Toxins · doi:10.3390/toxins14030184 · Cited by 19 · see citing works
Loh, M. K., Stickling, C. P., Schrank, S., Hanshaw, M., Ritger, A. C., Dilosa, N., Finlay, J., Ferrara, N. C., & Rosenkranz, J. A. (2023) · Psychopharmacology · doi:10.1007/s00213-023-06308-8 · Cited by 17 · see citing works
Specialization of amygdala subregions in emotion processing
Labuschagne, I., Domínguez, J. F., Grace, S., Mizzi, S., Henry, J. D., Peters, C. A., Rabinak, C. A., Sinclair, E., Lorenzetti, V., Terrett, G., et al. (2024) · Human Brain Mapping · doi:10.1002/hbm.26673 · Cited by 17 · see citing works
Bolshakov, A. P., Stepanichev, M. Y., Dobryakova, Y. V., Spivak, Y. S., & Markevich, V. A. (2020) · Toxins · doi:10.3390/toxins12090546 · Cited by 17 · see citing works
Modeling Interneuron Dysfunction in Schizophrenia
Schmidt, M. J., & Mirnics, K. (2012) · Developmental Neuroscience · doi:10.1159/000336731 · Cited by 17 · see citing works
Psychosocial impairment following mild blast-induced traumatic brain injury in rats
Race, N. S., Andrews, K. D., Lungwitz, E. A., Vega‐Alvarez, S., Warner, T. R., Acosta, G., Cao, J., Lu, K., Liu, Z., Dietrich, A. D., et al. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113405 · Cited by 16 · see citing works
Self-citationPhysiology of the Amygdala: Implications for PTSD
Rainnie, D. G., & Ressler, K. J. (2009) · Humana Press eBooks · doi:10.1007/978-1-60327-329-9_3 · Cited by 13 · see citing works
Przybysz, K. R., Spodnick, M. B., Johnson, J. M., Varlinskaya, E. I., & Diaz, M. R. (2022) · Addiction Biology · doi:10.1111/adb.13252 · Cited by 10 · see citing works
Hauser, S. R., Deehan, G., Knight, C. P., Waeiss, R. A., Engleman, E., Ding, Z.-M., Johnson, P. L., Mcbride, W., Truitt, W., & Rodd, Z. (2023) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2023.109858 · Cited by 7 · see citing works
Self-citationJanetsian-Fritz, S. S., McCane, A. M., Linsenbardt, D. N., & Lapish, C. C. (2015) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000158 · Cited by 10 · see citing works
Burke, A. R., Bernabe, C., Dietrich, A. D., Daugherty, R. C., Lukkes, J. L., & Truitt, W. A. (2025) · Behavioural Brain Research · doi:10.1016/j.bbr.2025.115481 · Cited by 7 · see citing works
Self-citationSeillier, A., & Giuffrida, A. (2017) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000325 · Cited by 8 · see citing works
Gennarelli, M., Monteleone, P., Minelli, A., Monteleone, A. M., Rossi, A., Rocca, P., Bertolino, A., Aguglia, E., Amore, M., Bellino, S., et al. (2021) · World Journal of Biological Psychiatry · doi:10.1080/15622975.2021.1907722 · Cited by 8 · see citing works
Johnson, R. T., Breedlove, M., & Jordan, C. L. (2010) · Vitamins and hormones · doi:10.1016/s0083-6729(10)82002-3 · Cited by 7 · see citing works
Aerts, T., Boonen, A., Geenen, L., Stulens, A., Masin, L., Pancho, A., Francis, A., Pepermans, E., Baggerman, G., Roy, F. M. V., et al. (2024) · Open Biology · doi:10.1098/rsob.240113 · Cited by 5 · see citing works
Animal Models to Investigate Social Support Induced Anxiety Reductions
Majumdar, S., Lungwitz, E. A., Andrews, K. D., Chambers, J. E., & Truitt, W. A. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-813693-5.00012-5 · Cited by 5 · see citing works
Self-citationRole of Basolateral Amygdalar Somatostatin 2 Receptors in a Rat Model of Chronic Anxiety
Gaskins, D. L., Burke, A. R., Sajdyk, T. J., Truitt, W. A., Dietrich, A. D., & Shekhar, A. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.08.031 · Cited by 4 · see citing works
Self-citationMartin, B. S., & Huntsman, M. M. (2014) · The Receptors · doi:10.1007/978-1-4939-1426-5_13 · Cited by 2 · see citing works
Autism Spectrum Disorder, Fear Response, and Environmental Exposures
Theoharides, T. C., Sant, J., & Giota, M.-E. (2019) · Advances in human services and public health (AHSPH) book series · doi:10.4018/978-1-5225-7635-8.ch002 · Cited by 1 · see citing works
Sargent, K. (2022) · Digital Archive @ GSU · doi:10.57709/7282109
Bassi, G. S. (2012) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/d.59.2012.tde-01062012-144552
THE EFFECT OF ETHANOL ON IMPULSIVITY IN HIGH ALCOHOL PREFERRING MICE
Oberlin, B. G. (2010) · IUScholarWorks (Indiana University) · doi:10.7912/c2/2040
Self-citationGaskins, D. L. (2012) · IUScholarWorks (Indiana University) · doi:10.7912/c2/2044
Janetsian-Fritz, S. S. (2014) · Purdue e-Pubs (Purdue University System) · doi:10.7912/c2/1087
Zhang, Y., Sack, A.-S., Jones, K. L., Yang, Y., Garcia, E., & Snutch, T. P. (2022) · eNeuro · doi:10.1523/eneuro.0282-21.2022
Przybysz, K. R., Spodnick, M. B., Johnson, J. M., Varlinskaya, E. I., & Diaz, M. R. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.05.02.490324
Chavez, M. C., Jones, M. M., Whaley, A. R., Pounders, T. M., Tremblay, J. T., Zajkowski, M., Ragusa, M., Lau, B. Y. B., & Schulz, K. M. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.07.31.667823
Chavez, M. C., Jones, M. M., Whaley, A. R., Pounders, T. M., Tremblay, J. T., Zajkowski, M. E., Ragusa, M., Lau, B. Y. B., & Schulz, K. M. (2025) · SSRN Electronic Journal · doi:10.2139/ssrn.5390441
Chavez, M. C., Jones, M. M., Whaley, A. R., Pounders, T. M., Tremblay, J. T., Zajkowski, M. E., Ragusa, M., Lau, B. Y. B., & Schulz, K. M. (2025) · SSRN Electronic Journal · doi:10.2139/ssrn.5390440
Hauser, S. R., Deehan, G., Knight, C. P., Waeiss, R. A., Engleman, E., Johnson, P. L., McBride, W. J., Bell, R. L., Truitt, W., & Rodd, Z. (2025) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2025.1634350
Self-citationBehavioral Effects of Agmatine in a Valproic Acid-Induced Rat Model of Autism Spectrum Disorder
Arıcıoğlu, F., Kabacaoğlu, G., Korkmaz, E., Bahtiyar, B. C., Sümer, E., & Yılmaz, B. (2025) · Clinical and Experimental Health Sciences · doi:10.33808/clinexphealthsci.1812820
Chavez, M. C., Tremblay, J. T., Zajkowski, M. E., Ragusa, M., Jones, M. M., Whaley, A. R., Pounders, T. M., Lau, B. Y. B., & Schulz, K. M. (2026) · Brain Research · doi:10.1016/j.brainres.2026.150264
- Authors
- Truitt, W. A., Sajdyk, T. J., Dietrich, A. D., Oberlin, B., McDougle, C. J., & Shekhar, A.
- Affiliations
- Indiana University School of Medicine (US)
- Corresponding author
- Shekhar, Anantha
- Venue
- Psychopharmacology
- Published
- 2007-02-03
- Volume
- 191
- Issue
- 1
- Pages
- 107-118
- ISSN
- 0033-3158 (ISSN-L)
- 1432-2072
- OpenAlex
- W2054166255
- Cited by
- 79
- References
- 88
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 2 · 2023: 3 · 2022: 7 · 2021: 6 · 2020: 2 · 2019: 4 · 2018: 4 · 2017: 4 · 2016: 1 · 2015: 5 · 2014: 6 · 2013: 7 · 2012: 4
- FWCI
- 1.67
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Psychopharmacology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (R01-MH52619, R01-MH65702, R01MH052619, R01MH065702)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- basolateral amygdala, GABAergic interneurons, inhibitory tone, social anxiety, autism spectrum disorder, social interaction, urocortin 1, corticotropin-releasing factor, neurokinin-1 receptor, ventromedial prefrontal cortex, c-fos, social inhibition, habituation, animal models of psychiatric disorders
- MeSH terms
- Saporins, Amygdala, Animals, Anxiety, Autistic Disorder, Behavior, Animal, Corticotropin-Releasing Hormone, Disease Models, Animal, Habituation, Psychophysiologic, Interneurons, Male, Neural Inhibition, Neural Pathways, Recombinant Fusion Proteins, Social Behavior, Social Behavior Disorders, Time Factors, Rats, Wistar, Prefrontal Cortex, Receptors, Corticotropin-Releasing Hormone, Receptors, Neurokinin-1, Rats, Ribosome Inactivating Proteins, Type 1, Urocortins
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