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Published in: Brain Structure and Function 1/2017

01-01-2017 | Original Article

A role for the anteromedial thalamic nucleus in the acquisition of contextual fear memory to predatory threats

Authors: Miguel Antonio Xavier de Lima, Marcus Vinicius C. Baldo, Newton Sabino Canteras

Published in: Brain Structure and Function | Issue 1/2017

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Abstract

Previous studies from our group have shown that cytotoxic lesions in the ventral portion of the anteromedial thalamic nucleus (AMv), one of the main targets of the hypothalamic predator-responsive circuit, strongly impairs contextual fear responses to an environment previously associated with a predator. The AMv is in a position to convey information to cortico-hippocampal-amygdalar circuits involved in the processing of fear memory. However, it remains to be determined whether the nucleus is involved in the acquisition or subsequent expression of contextual fear. In the present investigation, we addressed this question by inactivating the rat AMv with muscimol either prior to cat exposure or prior to exposure to the cat-related context. Accordingly, AMv pharmacological inactivation prior to cat exposure did not interfere with innate fear responses, but it drastically reduced contextual conditioning to the predator-associated environment. On the other hand, AMv inactivation prior to exposure to the environment associated with the predator threat did not affect contextual fear responses. The behavioral results were further supported by the demonstration that AMv inactivation prior to cat exposure also blocked the activation of sites critically involved in the expression of anti-predatory contextual defensive responses (i.e., the dorsal premammillary nucleus and the dorsolateral periaqueductal gray) in animals exposed to the predator-associated context. The AMv projections were also examined, and the results of this investigation outline important paths that can influence hippocampal circuitry and raise new ideas for anterior thalamic-hippocampal paths involved in emotional learning.
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Literature
go back to reference Aggleton JP, Hunt PR, Nagle S, Neave N (1996) The effects of selective lesions within the anterior thalamic nuclei on spatial memory in the rat. Behav Brain Res 81:189–198CrossRefPubMed Aggleton JP, Hunt PR, Nagle S, Neave N (1996) The effects of selective lesions within the anterior thalamic nuclei on spatial memory in the rat. Behav Brain Res 81:189–198CrossRefPubMed
go back to reference Aggleton JP, O’Mara SM, Vann SD, Wright NF, Tsanov M, Erichsen JT (2010) Hippocampal-anterior thalamic pathways for memory: uncovering a network of direct and indirect actions. Eur J Neurosci 31:2292–2307CrossRefPubMedPubMedCentral Aggleton JP, O’Mara SM, Vann SD, Wright NF, Tsanov M, Erichsen JT (2010) Hippocampal-anterior thalamic pathways for memory: uncovering a network of direct and indirect actions. Eur J Neurosci 31:2292–2307CrossRefPubMedPubMedCentral
go back to reference Buzsaki G (2005) Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15:827–840CrossRefPubMed Buzsaki G (2005) Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15:827–840CrossRefPubMed
go back to reference Byatt G, Dalrymple-Alford JC (1996) Both anteromedial and anteroventral thalamic lesions impair radial maze learning in rats. Behav Neurosci 110:1335–1348CrossRefPubMed Byatt G, Dalrymple-Alford JC (1996) Both anteromedial and anteroventral thalamic lesions impair radial maze learning in rats. Behav Neurosci 110:1335–1348CrossRefPubMed
go back to reference Canteras NS, Kroon JAV, Do-Monte FHM, Pavesi E, Carobrez AP (2008) Sensing danger through the olfactory system: the role of the hypothalamicdorsal premammillary nucleus. Neurosci Biobehav Rev 32:1228–1235CrossRefPubMed Canteras NS, Kroon JAV, Do-Monte FHM, Pavesi E, Carobrez AP (2008) Sensing danger through the olfactory system: the role of the hypothalamicdorsal premammillary nucleus. Neurosci Biobehav Rev 32:1228–1235CrossRefPubMed
go back to reference Carlesimo GA, Lombardi MG, Caltagirone C (2011) Vascular thalamic amnesia: a reappraisal. Neuropsychologia 49:777–789CrossRefPubMed Carlesimo GA, Lombardi MG, Caltagirone C (2011) Vascular thalamic amnesia: a reappraisal. Neuropsychologia 49:777–789CrossRefPubMed
go back to reference Carvalho-Netto EF, Martinez RC, Baldo MV, Canteras NS (2010) Evidence for the thalamic targets of the medial hypothalamic defensive system mediating emotional memory to predatory threats. Neurobiol Learn Mem 93:479–486CrossRefPubMed Carvalho-Netto EF, Martinez RC, Baldo MV, Canteras NS (2010) Evidence for the thalamic targets of the medial hypothalamic defensive system mediating emotional memory to predatory threats. Neurobiol Learn Mem 93:479–486CrossRefPubMed
go back to reference Cezario A, Ribeiro-Barbosa E, Baldo M, Canteras N (2008) Hypothalamic sites responding to predator threats—the role of the dorsal premammillary nucleus in unconditioned and conditioned antipredatory defensive behavior. Eur J Neurosci 28:1003–1015CrossRefPubMed Cezario A, Ribeiro-Barbosa E, Baldo M, Canteras N (2008) Hypothalamic sites responding to predator threats—the role of the dorsal premammillary nucleus in unconditioned and conditioned antipredatory defensive behavior. Eur J Neurosci 28:1003–1015CrossRefPubMed
go back to reference Clark BJ, Taube JS (2011) Intact landmark control and angular path integration by head direction cells in the anterodorsal thalamus after lesions of the medial entorhinal cortex. Hippocampus 21:767–782CrossRefPubMed Clark BJ, Taube JS (2011) Intact landmark control and angular path integration by head direction cells in the anterodorsal thalamus after lesions of the medial entorhinal cortex. Hippocampus 21:767–782CrossRefPubMed
go back to reference Dielenberg RA, Hunt GE, McGregor IS (2001) ‘‘When a rat smells a cat”: the distribution of Fos immunoreactivity in rat brain following exposure to a predatory odor. Neuroscience 104:1085–1097CrossRefPubMed Dielenberg RA, Hunt GE, McGregor IS (2001) ‘‘When a rat smells a cat”: the distribution of Fos immunoreactivity in rat brain following exposure to a predatory odor. Neuroscience 104:1085–1097CrossRefPubMed
go back to reference Ding S-L (2013) Comparative anatomy of the prosubiculum, subiculum, presubiculum, postsubiculum, and parasubiculum in human, monkey, and rodent. J Comp Neurol 521:4145–4162CrossRefPubMed Ding S-L (2013) Comparative anatomy of the prosubiculum, subiculum, presubiculum, postsubiculum, and parasubiculum in human, monkey, and rodent. J Comp Neurol 521:4145–4162CrossRefPubMed
go back to reference Do Monte FH, Canteras NS, Fernandes D, Assreuy J, Carobrez AP (2008) New perspectives on beta-adrenergic mediation of innate and learned fear responses to predator odor. J Neurosci 28:13296–13302CrossRefPubMed Do Monte FH, Canteras NS, Fernandes D, Assreuy J, Carobrez AP (2008) New perspectives on beta-adrenergic mediation of innate and learned fear responses to predator odor. J Neurosci 28:13296–13302CrossRefPubMed
go back to reference Dupire A, Kant P, Mons N, Marchand AR, Coutureau E, Dalrymple-Alford J, Wolff M (2013) A role for anterior thalamic nuclei in affective cognition: inter-action with environmental conditions. Hippocampus 23:392–404CrossRefPubMed Dupire A, Kant P, Mons N, Marchand AR, Coutureau E, Dalrymple-Alford J, Wolff M (2013) A role for anterior thalamic nuclei in affective cognition: inter-action with environmental conditions. Hippocampus 23:392–404CrossRefPubMed
go back to reference Harding A, Halliday G, Caine D, Kril J (2000) Degeneration of anterior thalamic nuclei differentiates alcoholics with amnesia. Brain 123:141–154CrossRefPubMed Harding A, Halliday G, Caine D, Kril J (2000) Degeneration of anterior thalamic nuclei differentiates alcoholics with amnesia. Brain 123:141–154CrossRefPubMed
go back to reference Herkenham M (1978) The connections of the nucleus reuniens thalami: evidence for a direct thalamo-hippocampal pathway in the rat. J Comp Neurol 177:589–610CrossRefPubMed Herkenham M (1978) The connections of the nucleus reuniens thalami: evidence for a direct thalamo-hippocampal pathway in the rat. J Comp Neurol 177:589–610CrossRefPubMed
go back to reference Jankowski MM, Ronnqvist KC, Tsanov M, Vann SD, Wright NF, Erichsen JT, Aggleton JP, O’Mara SM (2013) The anterior thalamus provides a subcortical circuit supporting memory and spatial navigation. Front Syst Neurosci 7:45CrossRefPubMedPubMedCentral Jankowski MM, Ronnqvist KC, Tsanov M, Vann SD, Wright NF, Erichsen JT, Aggleton JP, O’Mara SM (2013) The anterior thalamus provides a subcortical circuit supporting memory and spatial navigation. Front Syst Neurosci 7:45CrossRefPubMedPubMedCentral
go back to reference Jones BF, Witter MP (2007) Cingulate cortex projections to the parahippocampal region and hippocampal formation in the rat. Hippocampus 17:957–976CrossRefPubMed Jones BF, Witter MP (2007) Cingulate cortex projections to the parahippocampal region and hippocampal formation in the rat. Hippocampus 17:957–976CrossRefPubMed
go back to reference Law LM, Smith DM (2012) The anterior thalamus is critical for overcoming interference in a context-dependent odor discrimination task. Behav Neurosci 126:710–719CrossRefPubMedPubMedCentral Law LM, Smith DM (2012) The anterior thalamus is critical for overcoming interference in a context-dependent odor discrimination task. Behav Neurosci 126:710–719CrossRefPubMedPubMedCentral
go back to reference Marchand A, Faugère A, Coutureau E, Wolff M (2014) A role for anterior thalamic nuclei in contextual fear memory. Brain Struct Funct 219:1575–1586CrossRefPubMed Marchand A, Faugère A, Coutureau E, Wolff M (2014) A role for anterior thalamic nuclei in contextual fear memory. Brain Struct Funct 219:1575–1586CrossRefPubMed
go back to reference Martinez RC, Carvalho-Netto EF, Ribeiro-Barbosa ER, Baldo MV, Canteras NS (2011) Amygdalar roles during exposure to a live predator and to a predator-associated context. Neuroscience 172:314–328CrossRefPubMed Martinez RC, Carvalho-Netto EF, Ribeiro-Barbosa ER, Baldo MV, Canteras NS (2011) Amygdalar roles during exposure to a live predator and to a predator-associated context. Neuroscience 172:314–328CrossRefPubMed
go back to reference Papez JW (1937) A proposed mechanism of emotion. Arch Neur Psych 38:725–743CrossRef Papez JW (1937) A proposed mechanism of emotion. Arch Neur Psych 38:725–743CrossRef
go back to reference Pentkowski NS, Blanchard DC, Lever C, Litvin Y, Blanchard RJ (2006) Effects of lesions to the dorsal and ventral hippocampus on defensive behaviors in rats. Eur J Neurosci 23:2185–2196CrossRefPubMed Pentkowski NS, Blanchard DC, Lever C, Litvin Y, Blanchard RJ (2006) Effects of lesions to the dorsal and ventral hippocampus on defensive behaviors in rats. Eur J Neurosci 23:2185–2196CrossRefPubMed
go back to reference Ribeiro-Barbosa ER, Canteras NS, Cezario AF, Blanchard RJ, Blanchard DC (2005) An alternative experimental procedure for studying predator related defensive responses. Neurosci Biobehav Rev 29:1255–1263CrossRefPubMed Ribeiro-Barbosa ER, Canteras NS, Cezario AF, Blanchard RJ, Blanchard DC (2005) An alternative experimental procedure for studying predator related defensive responses. Neurosci Biobehav Rev 29:1255–1263CrossRefPubMed
go back to reference Shi C-J, Cassell MD (1999) Perirhinal cortex projections to the amygdaloid complex and hippocampal formation in the rat. J Comp Neurol 406:299–328CrossRefPubMed Shi C-J, Cassell MD (1999) Perirhinal cortex projections to the amygdaloid complex and hippocampal formation in the rat. J Comp Neurol 406:299–328CrossRefPubMed
go back to reference Shibata H (1993a) Efferent projections from the anterior thalamic nuclei to the cingulate cortex in the rat. J Comp Neurol 330:533–542CrossRefPubMed Shibata H (1993a) Efferent projections from the anterior thalamic nuclei to the cingulate cortex in the rat. J Comp Neurol 330:533–542CrossRefPubMed
go back to reference Shibata H (1993b) Direct projections from the anterior thalamic nuclei to the retrohippocampal region in the rat. J Comp Neurol 337:431–445CrossRefPubMed Shibata H (1993b) Direct projections from the anterior thalamic nuclei to the retrohippocampal region in the rat. J Comp Neurol 337:431–445CrossRefPubMed
go back to reference Swanson LW (2004) Brain maps: structure of the rat brain. Elsevier, Amsterdam Swanson LW (2004) Brain maps: structure of the rat brain. Elsevier, Amsterdam
go back to reference Swanson LW, Köhler C, Björklund A (1987) The limbic region. I: the septohippocampal system. In: Hökfelt T, Björklund A, Swanson LW (eds) Handbook of chemical neuroanatomy. Integrated systems, vol 5. Elsevier, Amsterdam, pp 125–277 Swanson LW, Köhler C, Björklund A (1987) The limbic region. I: the septohippocampal system. In: Hökfelt T, Björklund A, Swanson LW (eds) Handbook of chemical neuroanatomy. Integrated systems, vol 5. Elsevier, Amsterdam, pp 125–277
go back to reference Taube JS (1995) Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J Neurosci 15:70–86PubMed Taube JS (1995) Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J Neurosci 15:70–86PubMed
go back to reference Tsanov M, Chah E, Wright N, Vann SD, Reilly R, Erichsen JT, Aggleton JP, O’Mara SM (2011) Oscillatory entrainment of thalamic neurons by theta rhythm in freely moving rats. J Neurophysiol 105:4–17CrossRefPubMed Tsanov M, Chah E, Wright N, Vann SD, Reilly R, Erichsen JT, Aggleton JP, O’Mara SM (2011) Oscillatory entrainment of thalamic neurons by theta rhythm in freely moving rats. J Neurophysiol 105:4–17CrossRefPubMed
go back to reference Tsivilis D, Vann SD, Denby C, Roberts N, Mayes AR, Montaldi D, Aggleton JP (2008) A disproportionate role for the fornix and mammillary bodies in recall versus recognition memory. Nat Neurosci 11:834–842CrossRefPubMed Tsivilis D, Vann SD, Denby C, Roberts N, Mayes AR, Montaldi D, Aggleton JP (2008) A disproportionate role for the fornix and mammillary bodies in recall versus recognition memory. Nat Neurosci 11:834–842CrossRefPubMed
go back to reference Van Groen T, Kadish I, Wyss JM (1999) Efferent connections of the anteromedial nucleus of the thalamus of the rat. Brain Res Rev 30:1–26CrossRefPubMed Van Groen T, Kadish I, Wyss JM (1999) Efferent connections of the anteromedial nucleus of the thalamus of the rat. Brain Res Rev 30:1–26CrossRefPubMed
go back to reference Vertes RP, Albo Z, Viana Di Prisco G (2001) Theta-rhythmically firing neurons in the anterior thalamus: implications for mnemonic functions of Papez’s circuit. Neuroscience 104:619–625CrossRefPubMed Vertes RP, Albo Z, Viana Di Prisco G (2001) Theta-rhythmically firing neurons in the anterior thalamus: implications for mnemonic functions of Papez’s circuit. Neuroscience 104:619–625CrossRefPubMed
go back to reference Vertes RP, Hoover WB, Do Valle AC, Sherman A, Rodriguez JJ (2006) Efferent projections of reuniens and rhomboid nuclei of the thalamus in the rat. J Comp Neurol 499:768–796CrossRefPubMed Vertes RP, Hoover WB, Do Valle AC, Sherman A, Rodriguez JJ (2006) Efferent projections of reuniens and rhomboid nuclei of the thalamus in the rat. J Comp Neurol 499:768–796CrossRefPubMed
go back to reference Wolff M, Gibb SJ, Dalrymple-Alford JC (2006) Beyond spatial memory: the anterior thalamus and memory for the temporal order of a sequence of odor cues. J Neurosci 26:2907–2913CrossRefPubMed Wolff M, Gibb SJ, Dalrymple-Alford JC (2006) Beyond spatial memory: the anterior thalamus and memory for the temporal order of a sequence of odor cues. J Neurosci 26:2907–2913CrossRefPubMed
go back to reference Wolff M, Alcaraz F, Marchand AR, Coutureau E (2015) Functional heterogeneity of the limbic thalamus: from hippocampal to cortical functions. Neurosci Biobehav Rev 54:120–130CrossRefPubMed Wolff M, Alcaraz F, Marchand AR, Coutureau E (2015) Functional heterogeneity of the limbic thalamus: from hippocampal to cortical functions. Neurosci Biobehav Rev 54:120–130CrossRefPubMed
Metadata
Title
A role for the anteromedial thalamic nucleus in the acquisition of contextual fear memory to predatory threats
Authors
Miguel Antonio Xavier de Lima
Marcus Vinicius C. Baldo
Newton Sabino Canteras
Publication date
01-01-2017
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 1/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-016-1204-2

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