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Published in: Brain Structure and Function 1/2012

01-01-2012 | Original Article

Synaptology of ventral CA1 and subiculum projections to the basomedial nucleus of the amygdala in the mouse: relation to GABAergic interneurons

Authors: M. Müller, H. Faber-Zuschratter, Y. Yanagawa, O. Stork, H. Schwegler, Rüdiger Linke

Published in: Brain Structure and Function | Issue 1/2012

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Abstract

GABAergic neurons of the amygdala are thought to play a critical role in establishing networks for feedback and feedforward inhibition and in mediating rhythmic network activity patterns relevant for emotional behavior, determination of stimulus salience, and memory strength under stressful experiences. These functions are typically fulfilled in interplay of amygdala and hippocampus. Therefore, we explored the putative connectivity of GABAergic neurons with the hippocampo-amygdalar projection with the anterograde tracers Phaseolus vulgaris leucoagglutinin (Phal) and Miniruby injected to GAD67-GFP knock-in mice in which GABAergic neurons are labeled by the expression of the gene for green fluorescent protein (GFP) inserted to the GAD1 gene locus (Tamamaki et al. J Comp Neurol 467:60–79, 2003). We found that, while hippocampal axons target all nuclei of the amygdala, the densest fiber plexus was found in the posterior basomedial nucleus. Electron microscopy revealed that the vast majority of contacts in this nucleus were formed by thin fibers making small asymmetrical contacts, predominantly on GFP-negative profiles. However, several asymmetrical contacts could also be seen on GFP-positive profiles. A surprising result was the occasional occurrence of anterogradely labeled symmetrical synapses indicating a GABAergic contribution to the projection from the hippocampus to the amygdala. While hippocampal input to the amygdala appears to be largely excitatory and targets non-GABAergic neurons, our data provide evidence for a direct involvement of GABAergic neurons in the interplay of these regions, either as target in the amygdala or as projection neurons from the hippocampus. These particular “interface neurons” may be of relevance for the information processing in the amygdalo-hippocampal system involved in emotional behavior and memory formation.
Literature
go back to reference Adams JC (1981) Heavy metal intensification of DAB-based HRP reaction product. J Histochem Cytochem 29:775PubMedCrossRef Adams JC (1981) Heavy metal intensification of DAB-based HRP reaction product. J Histochem Cytochem 29:775PubMedCrossRef
go back to reference Albrecht A, Bergado-Acosta JR, Pape HC, Stork O (2010) Role of the neural cell adhesion molecule (NCAM) in amygdalo-hippocampal interactions and salience determination of contextual fear memory. Int J Neuropsychopharmacol 13:661–674PubMedCrossRef Albrecht A, Bergado-Acosta JR, Pape HC, Stork O (2010) Role of the neural cell adhesion molecule (NCAM) in amygdalo-hippocampal interactions and salience determination of contextual fear memory. Int J Neuropsychopharmacol 13:661–674PubMedCrossRef
go back to reference Alvarez RP, Biggs A, Chen G, Pine DS, Grillon C (2008) contextual fear conditioning in humans: cortical-hippocampal and amygdala contributions. J Neurosci 28:6211–6219PubMedCrossRef Alvarez RP, Biggs A, Chen G, Pine DS, Grillon C (2008) contextual fear conditioning in humans: cortical-hippocampal and amygdala contributions. J Neurosci 28:6211–6219PubMedCrossRef
go back to reference Bergado-Acosta JR, Sangha S, Narayanan RT, Obata K, Pape HC, Stork O (2008) Critical role of the 65-kDa isoform of glutamic acid decarboxylase in consolidation and generalization of Pavlovian fear memory. Learn Mem 15:163–171PubMedCrossRef Bergado-Acosta JR, Sangha S, Narayanan RT, Obata K, Pape HC, Stork O (2008) Critical role of the 65-kDa isoform of glutamic acid decarboxylase in consolidation and generalization of Pavlovian fear memory. Learn Mem 15:163–171PubMedCrossRef
go back to reference Bissiere S, Humeau Y, Luthi A (2003) Dopamine gates LTP induction in lateral amygdala by suppressing feedforward inhibition. Nat Neurosci 6:587–592PubMedCrossRef Bissiere S, Humeau Y, Luthi A (2003) Dopamine gates LTP induction in lateral amygdala by suppressing feedforward inhibition. Nat Neurosci 6:587–592PubMedCrossRef
go back to reference Brinley-Reed M, Mascagni F, McDonald AJ (1995) Synaptology of prefrontal cortical projections to the basolateral amygdala: an electron microscopic study in the rat. Neurosci Lett 202:45–48PubMedCrossRef Brinley-Reed M, Mascagni F, McDonald AJ (1995) Synaptology of prefrontal cortical projections to the basolateral amygdala: an electron microscopic study in the rat. Neurosci Lett 202:45–48PubMedCrossRef
go back to reference Canteras NS, Swanson LW (1992) Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHA-L anterograde tract-tracing study in the rat. J Comp Neurol 324:180–194PubMedCrossRef Canteras NS, Swanson LW (1992) Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHA-L anterograde tract-tracing study in the rat. J Comp Neurol 324:180–194PubMedCrossRef
go back to reference Carlsen J (1988) Immunocytochemical localization of glutamate decarboxylase in the rat basolateral amygdaloid nucleus, with special reference to GABAergic innervation of amygdalostriatal projection neurons. J Comp Neurol 273:513–526PubMedCrossRef Carlsen J (1988) Immunocytochemical localization of glutamate decarboxylase in the rat basolateral amygdaloid nucleus, with special reference to GABAergic innervation of amygdalostriatal projection neurons. J Comp Neurol 273:513–526PubMedCrossRef
go back to reference Carlsen J, Heimer L (1988) The basolateral amygdaloid complex as a cortical-like structure. Brain Res 441:377–380PubMedCrossRef Carlsen J, Heimer L (1988) The basolateral amygdaloid complex as a cortical-like structure. Brain Res 441:377–380PubMedCrossRef
go back to reference Cenquizca LA, Swanson LW (2007) Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex. Brain Res Rev 56:1–26PubMedCrossRef Cenquizca LA, Swanson LW (2007) Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex. Brain Res Rev 56:1–26PubMedCrossRef
go back to reference Chen S, Aston-Jones G (1998) Axonal collateral-collateral transport of tract tracers in brain neurons: false anterograde labelling and useful tool. Neuroscience 82:1151–1163PubMedCrossRef Chen S, Aston-Jones G (1998) Axonal collateral-collateral transport of tract tracers in brain neurons: false anterograde labelling and useful tool. Neuroscience 82:1151–1163PubMedCrossRef
go back to reference Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, Lüthi A (2009) Amygdala inhibitory circuits and the control of fear memory. Neuron 62:757–771PubMedCrossRef Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, Lüthi A (2009) Amygdala inhibitory circuits and the control of fear memory. Neuron 62:757–771PubMedCrossRef
go back to reference Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7–19PubMedCrossRef Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7–19PubMedCrossRef
go back to reference Franklin KBJ, Paxinos G (2007) The mouse brain in stereotaxic coordinates. Elsevier, New York Franklin KBJ, Paxinos G (2007) The mouse brain in stereotaxic coordinates. Elsevier, New York
go back to reference Gerfen CR, Sawchenko PE (1984) An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: Immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris Leucoagglutinin (PHA-L). Brain Res 290:219–238PubMedCrossRef Gerfen CR, Sawchenko PE (1984) An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: Immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris Leucoagglutinin (PHA-L). Brain Res 290:219–238PubMedCrossRef
go back to reference Groenewegen HJ, Wouterlood FG (1990) Light and electron microscopic tracing of neuronal connections with Phaseolus vulgaris-leucoagglutinin (PHA-L), and combinations with other neuroanatomical techniques. In: Björklund A, Hökfelt T, Wouterlood FG, van den Pol AN (eds) Handbook of chemical neuroanatomy, Vol. 8: Analysis of neuronal microcircuits and synaptic interactions. Elsevier Science Publishers B.V, Amsterdam, pp 47–124 Groenewegen HJ, Wouterlood FG (1990) Light and electron microscopic tracing of neuronal connections with Phaseolus vulgaris-leucoagglutinin (PHA-L), and combinations with other neuroanatomical techniques. In: Björklund A, Hökfelt T, Wouterlood FG, van den Pol AN (eds) Handbook of chemical neuroanatomy, Vol. 8: Analysis of neuronal microcircuits and synaptic interactions. Elsevier Science Publishers B.V, Amsterdam, pp 47–124
go back to reference Hajos F, Staiger JF, Halasy K, Freund TF, Zilles K (1997) Geniculo-cortical afferents form synaptic contacts with vasoactive intestinal polypeptide (VIP) immunoreactive neurons of the rat visual cortex. Neurosci Lett 228:179–182PubMedCrossRef Hajos F, Staiger JF, Halasy K, Freund TF, Zilles K (1997) Geniculo-cortical afferents form synaptic contacts with vasoactive intestinal polypeptide (VIP) immunoreactive neurons of the rat visual cortex. Neurosci Lett 228:179–182PubMedCrossRef
go back to reference Han JH, Kushner SA, Yiu AP, Cole CJ, Matynia A, Brown RA, Neve RL, Guzowski JF, Silva AJ, Josselyn SA (2007) Neuronal competition and selection during memory formation. Science 316:457–460PubMedCrossRef Han JH, Kushner SA, Yiu AP, Cole CJ, Matynia A, Brown RA, Neve RL, Guzowski JF, Silva AJ, Josselyn SA (2007) Neuronal competition and selection during memory formation. Science 316:457–460PubMedCrossRef
go back to reference Herry C, Ciocchi S, Senn V, Demmou L, Muller C, Lüthi A (2008) Switching on and off fear by distinct neuronal circuits. Nature 454:600–606PubMedCrossRef Herry C, Ciocchi S, Senn V, Demmou L, Muller C, Lüthi A (2008) Switching on and off fear by distinct neuronal circuits. Nature 454:600–606PubMedCrossRef
go back to reference Hobin JA, Ji J, Maren S (2006) Ventral hippocampal muscimol disrupts context-specific fear memory retrieval after extinction in rats. Hippocampus 16:174–182PubMedCrossRef Hobin JA, Ji J, Maren S (2006) Ventral hippocampal muscimol disrupts context-specific fear memory retrieval after extinction in rats. Hippocampus 16:174–182PubMedCrossRef
go back to reference Ji J, Maren S (2007) Hippocampal involvement in contextual modulation of fear extinction. Hippocampus 17:749–758PubMedCrossRef Ji J, Maren S (2007) Hippocampal involvement in contextual modulation of fear extinction. Hippocampus 17:749–758PubMedCrossRef
go back to reference Jinno S, Klausberger T, Marton LF, Dalezios Y, Roberts JD, Fuentealba P, Bushong EA, Henze D, Buzsaki G, Somogyi P (2007) Neuronal diversity in GABAergic long-range projections from the hippocampus. J Neurosci 27:8790–8804PubMedCrossRef Jinno S, Klausberger T, Marton LF, Dalezios Y, Roberts JD, Fuentealba P, Bushong EA, Henze D, Buzsaki G, Somogyi P (2007) Neuronal diversity in GABAergic long-range projections from the hippocampus. J Neurosci 27:8790–8804PubMedCrossRef
go back to reference Kaneko K, Tamamaki N, Owada H, Kakizaki T, Kume N, Totsuka M, Yamamoto T, Yawo H, Yagi T, Obata K, Yanagawa Y (2008) Noradrenergic excitation of a subpopulation of GABAergic cells in the basolateral amygdala via both activation of nonselective cationic conductance and suppression of resting K+ conductance: a study using glutamate decarboxylase 67-green fluorescent protein knock-in mice. Neuroscience 157:781–797PubMedCrossRef Kaneko K, Tamamaki N, Owada H, Kakizaki T, Kume N, Totsuka M, Yamamoto T, Yawo H, Yagi T, Obata K, Yanagawa Y (2008) Noradrenergic excitation of a subpopulation of GABAergic cells in the basolateral amygdala via both activation of nonselective cationic conductance and suppression of resting K+ conductance: a study using glutamate decarboxylase 67-green fluorescent protein knock-in mice. Neuroscience 157:781–797PubMedCrossRef
go back to reference Kishi T, Tsumori T, Yokota S, Yasui Y (2006) Topographical projection from the hippocampal formation to the amygdala: a combined anterograde and retrograde tracing study in the rat. J Comp Neurol 496:349–368PubMedCrossRef Kishi T, Tsumori T, Yokota S, Yasui Y (2006) Topographical projection from the hippocampal formation to the amygdala: a combined anterograde and retrograde tracing study in the rat. J Comp Neurol 496:349–368PubMedCrossRef
go back to reference Lanciego JL, Wouterlood FG (2006) Multiple neuroanatomical tract-tracing: approaches for multiple tract tracing. In: Zaborszky L, Wouterlood FG, Lanciego JL (eds) Neuroanatomical tract-tracing 3. Molecules, neurons, and systems. Springer, New York, pp 336–363CrossRef Lanciego JL, Wouterlood FG (2006) Multiple neuroanatomical tract-tracing: approaches for multiple tract tracing. In: Zaborszky L, Wouterlood FG, Lanciego JL (eds) Neuroanatomical tract-tracing 3. Molecules, neurons, and systems. Springer, New York, pp 336–363CrossRef
go back to reference LeDoux JE, Farb CR, Milner TA (1991) Ultrastructure and synaptic associations of auditory thalamo-amygdala projections in the rat. Exp Brain Res 85:577–586PubMedCrossRef LeDoux JE, Farb CR, Milner TA (1991) Ultrastructure and synaptic associations of auditory thalamo-amygdala projections in the rat. Exp Brain Res 85:577–586PubMedCrossRef
go back to reference Li R, Nishijo H, Ono T, Ohtani Y, Ohtani O (2002) Synapses on GABAergic neurons in the basolateral nucleus of the rat amygdala: double-labeling immunoelectron microscopy. Synapse 43:42–50PubMedCrossRef Li R, Nishijo H, Ono T, Ohtani Y, Ohtani O (2002) Synapses on GABAergic neurons in the basolateral nucleus of the rat amygdala: double-labeling immunoelectron microscopy. Synapse 43:42–50PubMedCrossRef
go back to reference Makkar SR, Zhang SQ, Cranney J (2010) Behavioral and neural analysis of GABA in the acquisition, consolidation, reconsolidation, and extinction of fear memory. Neuropsychopharmacology 35:1625–1652PubMed Makkar SR, Zhang SQ, Cranney J (2010) Behavioral and neural analysis of GABA in the acquisition, consolidation, reconsolidation, and extinction of fear memory. Neuropsychopharmacology 35:1625–1652PubMed
go back to reference Maren S, Hobin JA (2007) Hippocampal regulation of context-dependent neuronal activity in the lateral amygdala. Learn Mem 14:318–324PubMedCrossRef Maren S, Hobin JA (2007) Hippocampal regulation of context-dependent neuronal activity in the lateral amygdala. Learn Mem 14:318–324PubMedCrossRef
go back to reference McDonald AJ (1982) Neurons of the lateral and basolateral amygdaloid nuclei: a Golgi study in the rat. J Comp Neurol 212:293–312PubMedCrossRef McDonald AJ (1982) Neurons of the lateral and basolateral amygdaloid nuclei: a Golgi study in the rat. J Comp Neurol 212:293–312PubMedCrossRef
go back to reference Meis S, Bergado-Acosta JR, Yanagawa Y, Obata K, Stork O, Munsch T (2008) Identification of a Neuropeptide S responsive circuitry shaping amygdala activity via the endopiriform nucleus. PLoS ONE 3(7):e2695. doi:10.1371/journal.pone.0002695 Meis S, Bergado-Acosta JR, Yanagawa Y, Obata K, Stork O, Munsch T (2008) Identification of a Neuropeptide S responsive circuitry shaping amygdala activity via the endopiriform nucleus. PLoS ONE 3(7):e2695. doi:10.​1371/​journal.​pone.​0002695
go back to reference Muller JF, Mascagni F, McDonald AJ (2003) Synaptic connections of distinct interneuronal subpopulations in the rat basolateral amygdalar nucleus. J Comp Neurol 456:217–236PubMedCrossRef Muller JF, Mascagni F, McDonald AJ (2003) Synaptic connections of distinct interneuronal subpopulations in the rat basolateral amygdalar nucleus. J Comp Neurol 456:217–236PubMedCrossRef
go back to reference Muller JF, Mascagni F, McDonald AJ (2007) Serotonin-immunoreactive axon terminals innervate pyramidal cells and interneurons in the rat basolateral amygdala. J Comp Neurol 505:314–335PubMedCrossRef Muller JF, Mascagni F, McDonald AJ (2007) Serotonin-immunoreactive axon terminals innervate pyramidal cells and interneurons in the rat basolateral amygdala. J Comp Neurol 505:314–335PubMedCrossRef
go back to reference Muller JF, Mascagni F, McDonald AJ (2011) Cholinergic innervation of pyramidal cells and parvalbumin-immunoreactive interneurons in the rat basolateral amygdala. J Comp Neurol 519:790–805PubMedCrossRef Muller JF, Mascagni F, McDonald AJ (2011) Cholinergic innervation of pyramidal cells and parvalbumin-immunoreactive interneurons in the rat basolateral amygdala. J Comp Neurol 519:790–805PubMedCrossRef
go back to reference Ottersen OP (1982) Connections of the amygdala of the rat. IV. Corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase. J Comp Neurol 205:30–48PubMedCrossRef Ottersen OP (1982) Connections of the amygdala of the rat. IV. Corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase. J Comp Neurol 205:30–48PubMedCrossRef
go back to reference Pape HC, Pare D (2010) Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol Rev 90:419–463PubMedCrossRef Pape HC, Pare D (2010) Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol Rev 90:419–463PubMedCrossRef
go back to reference Peters A, Palay SL, Webster HD (1991) The fine structure of the nervous system. Oxford University Press, New York Peters A, Palay SL, Webster HD (1991) The fine structure of the nervous system. Oxford University Press, New York
go back to reference Pinard CR, Muller JF, Mascagni F, McDonald AJ (2008) Dopaminergic innervation of interneurons in the rat basolateral amygdala. Neuroscience 157:850–863PubMedCrossRef Pinard CR, Muller JF, Mascagni F, McDonald AJ (2008) Dopaminergic innervation of interneurons in the rat basolateral amygdala. Neuroscience 157:850–863PubMedCrossRef
go back to reference Pitkänen A, Pikkarainen M, Nurminen N, Ylinen A (2000) Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex. Ann N Y Acad Sci 911:369–391PubMedCrossRef Pitkänen A, Pikkarainen M, Nurminen N, Ylinen A (2000) Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex. Ann N Y Acad Sci 911:369–391PubMedCrossRef
go back to reference Rainnie DG, Asprodini EK, Shinnick-Gallagher P (1991) Inhibitory transmission in the basolateral amygdala. J Neurophysiol 66:999–1009PubMed Rainnie DG, Asprodini EK, Shinnick-Gallagher P (1991) Inhibitory transmission in the basolateral amygdala. J Neurophysiol 66:999–1009PubMed
go back to reference Repa JC, Muller J, Apergis J, Desrochers TM, Zhou Y, LeDoux JE (2001) Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat Neurosci 4:724–731PubMedCrossRef Repa JC, Muller J, Apergis J, Desrochers TM, Zhou Y, LeDoux JE (2001) Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat Neurosci 4:724–731PubMedCrossRef
go back to reference Richter-Levin G, Akirav I (2000) Amygdala-hippocampus dynamic interaction in relation to memory. Mol Neurobiol 22:11–20PubMedCrossRef Richter-Levin G, Akirav I (2000) Amygdala-hippocampus dynamic interaction in relation to memory. Mol Neurobiol 22:11–20PubMedCrossRef
go back to reference Roberts GW (1992) Neuropeptides: cellular morphology, major pathways, and functional considerations. In: Aggleton JP (ed) The amagdala. Neurobiological aspects of emotion, memory, amd mental dysfunction. Wiley-Liss, New York, pp 115–142 Roberts GW (1992) Neuropeptides: cellular morphology, major pathways, and functional considerations. In: Aggleton JP (ed) The amagdala. Neurobiological aspects of emotion, memory, amd mental dysfunction. Wiley-Liss, New York, pp 115–142
go back to reference Royer S, Martina M, Paré D (1999) An inhibitory interface gates impulse traffic between the input and output stations of the amygdala. J Neurosci 19:10575–10583PubMed Royer S, Martina M, Paré D (1999) An inhibitory interface gates impulse traffic between the input and output stations of the amygdala. J Neurosci 19:10575–10583PubMed
go back to reference Rudy JW, Matus-Amat P (2005) The ventral hippocampus supports a memory representation of context and contextual fear conditioning: implications for a unitary function of the hippocampus. Behav Neurosci 119:154–163PubMedCrossRef Rudy JW, Matus-Amat P (2005) The ventral hippocampus supports a memory representation of context and contextual fear conditioning: implications for a unitary function of the hippocampus. Behav Neurosci 119:154–163PubMedCrossRef
go back to reference Samson RD, Dumont EC, Pare D (2003) Feedback inhibition defines transverse processing modules in the lateral amygdala. J Neurosci 23:1966–1973PubMed Samson RD, Dumont EC, Pare D (2003) Feedback inhibition defines transverse processing modules in the lateral amygdala. J Neurosci 23:1966–1973PubMed
go back to reference Segal M, Richter-Levin G, Maggio N (2010) Stress-induced dynamic routing of hippocampal connectivity: a hypothesis. Hippocampus 20:1332–1338PubMedCrossRef Segal M, Richter-Levin G, Maggio N (2010) Stress-induced dynamic routing of hippocampal connectivity: a hypothesis. Hippocampus 20:1332–1338PubMedCrossRef
go back to reference Seidenbecher T, Laxmi TR, Stork O, Pape HC (2003) Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301:846–850PubMedCrossRef Seidenbecher T, Laxmi TR, Stork O, Pape HC (2003) Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301:846–850PubMedCrossRef
go back to reference Shaban H, Humeau Y, Herry C, Cassasus G, Shigemoto R, Ciocchi S, Barbieri S, van der Putten H, Kaupmann K, Bettler B, Lüthi A (2006) Generalization of amygdala LTP and conditioned fear in the absence of presynaptic inhibition. Nat Neurosci 9:1028–1035PubMedCrossRef Shaban H, Humeau Y, Herry C, Cassasus G, Shigemoto R, Ciocchi S, Barbieri S, van der Putten H, Kaupmann K, Bettler B, Lüthi A (2006) Generalization of amygdala LTP and conditioned fear in the absence of presynaptic inhibition. Nat Neurosci 9:1028–1035PubMedCrossRef
go back to reference Smith Y, Paré J-F, Paré D (1998) Cat intraamygdaloid inhibitory network: ultrastructural organization of parvalbumin-immunoreactive elements. J Comp Neurol 391:164–179PubMedCrossRef Smith Y, Paré J-F, Paré D (1998) Cat intraamygdaloid inhibitory network: ultrastructural organization of parvalbumin-immunoreactive elements. J Comp Neurol 391:164–179PubMedCrossRef
go back to reference Smith Y, Paré J-F, Paré D (2000) Differential innervation of parvalbumin-immunoreactive interneurons of the basolateral amygdaloid complex by cortical and intrinsic inputs. J Comp Neurol 416:496–508PubMedCrossRef Smith Y, Paré J-F, Paré D (2000) Differential innervation of parvalbumin-immunoreactive interneurons of the basolateral amygdaloid complex by cortical and intrinsic inputs. J Comp Neurol 416:496–508PubMedCrossRef
go back to reference Stoppel C, Albrecht A, Pape HC, Stork O (2006) Genes and neurons: molecular insights to fear and anxiety. Genes Brain Behav 5:34–47PubMedCrossRef Stoppel C, Albrecht A, Pape HC, Stork O (2006) Genes and neurons: molecular insights to fear and anxiety. Genes Brain Behav 5:34–47PubMedCrossRef
go back to reference Sutherland RJ, O’Brien J, Lehmann H (2008) Absence of systems consolidation of fear memories after dorsal, ventral, or complete hippocampal damage. Hippocampus 18:710–718PubMedCrossRef Sutherland RJ, O’Brien J, Lehmann H (2008) Absence of systems consolidation of fear memories after dorsal, ventral, or complete hippocampal damage. Hippocampus 18:710–718PubMedCrossRef
go back to reference Szinyei C, Heinbockel T, Montagne J, Pape H-C (2000) Putative cortical and thalamic inputs elicit convergent excitation in a population of GABAergic interneurons of the lateral amygdala. J Neurosci 20:8909–8915PubMed Szinyei C, Heinbockel T, Montagne J, Pape H-C (2000) Putative cortical and thalamic inputs elicit convergent excitation in a population of GABAergic interneurons of the lateral amygdala. J Neurosci 20:8909–8915PubMed
go back to reference Szinyei C, Stork O, Pape HC (2003) Contribution of NR2B subunits to synaptic transmission in amygdaloid interneurons. J Neurosci 23:2549–2556PubMed Szinyei C, Stork O, Pape HC (2003) Contribution of NR2B subunits to synaptic transmission in amygdaloid interneurons. J Neurosci 23:2549–2556PubMed
go back to reference Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J-I, Obata K, Kaneko T (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467:60–79PubMedCrossRef Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J-I, Obata K, Kaneko T (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467:60–79PubMedCrossRef
go back to reference Truitt WA, Johnson PL, Dietrich AD, Fitz SD, Shekhar A (2009) Anxiety-like behavior is modulated by a discrete subpopulation of interneurons in the basolateral amygdala. Neuroscience 160:284–294PubMedCrossRef Truitt WA, Johnson PL, Dietrich AD, Fitz SD, Shekhar A (2009) Anxiety-like behavior is modulated by a discrete subpopulation of interneurons in the basolateral amygdala. Neuroscience 160:284–294PubMedCrossRef
go back to reference Valverde F (1962) Intrinsic organization of the amygdaloid complex. A Golgi study in the mouse. Trab Inst Cajal Invest Biol 54:291–314 Valverde F (1962) Intrinsic organization of the amygdaloid complex. A Golgi study in the mouse. Trab Inst Cajal Invest Biol 54:291–314
go back to reference Van Groen T, Wyss JM (1990) Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections. J Comp Neurol 302:515–528PubMedCrossRef Van Groen T, Wyss JM (1990) Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections. J Comp Neurol 302:515–528PubMedCrossRef
go back to reference Woodruff AR, Sah P (2007a) Inhibition and synchronization of basal amygdala principal neuron spiking by parvalbumin-positive interneurons. J Neurophysiol 98:2956–2961PubMedCrossRef Woodruff AR, Sah P (2007a) Inhibition and synchronization of basal amygdala principal neuron spiking by parvalbumin-positive interneurons. J Neurophysiol 98:2956–2961PubMedCrossRef
go back to reference Woodruff AR, Sah P (2007b) Networks of parvalbumin-positive interneurons in the basolateral amygdala. J Neurosci 27:553–563PubMedCrossRef Woodruff AR, Sah P (2007b) Networks of parvalbumin-positive interneurons in the basolateral amygdala. J Neurosci 27:553–563PubMedCrossRef
go back to reference Wouterlood FG, Jorritsma-Byham B (1993) The anterograde neuroanatomical tracer biotinylated dextran-amine: comparison with the tracer Phaseolus vulgaris-leucoagglutinin in preparations for electron microscopy. J Neurosci Meth 48:75–87CrossRef Wouterlood FG, Jorritsma-Byham B (1993) The anterograde neuroanatomical tracer biotinylated dextran-amine: comparison with the tracer Phaseolus vulgaris-leucoagglutinin in preparations for electron microscopy. J Neurosci Meth 48:75–87CrossRef
go back to reference Yilmazer-Hanke DM, Hantsch M, Hanke J, Schulz C, Faber-Zuschratter H, Schwegler H (2004) Neonatal thyroxine treatment: changes in the number of corticotropin-releasing-factor (CRF) and neuropeptide Y (NPY) containing neurons and density of tyrosine hydroxylase positive fibers (TH) in the amygdala correlate with anxiety-related behavior of wistar rats. Neuroscience 124:283–297PubMedCrossRef Yilmazer-Hanke DM, Hantsch M, Hanke J, Schulz C, Faber-Zuschratter H, Schwegler H (2004) Neonatal thyroxine treatment: changes in the number of corticotropin-releasing-factor (CRF) and neuropeptide Y (NPY) containing neurons and density of tyrosine hydroxylase positive fibers (TH) in the amygdala correlate with anxiety-related behavior of wistar rats. Neuroscience 124:283–297PubMedCrossRef
Metadata
Title
Synaptology of ventral CA1 and subiculum projections to the basomedial nucleus of the amygdala in the mouse: relation to GABAergic interneurons
Authors
M. Müller
H. Faber-Zuschratter
Y. Yanagawa
O. Stork
H. Schwegler
Rüdiger Linke
Publication date
01-01-2012
Publisher
Springer-Verlag
Published in
Brain Structure and Function / Issue 1/2012
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-011-0326-9

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