Skip to main content
Erschienen in: Brain Structure and Function 5/2014

01.09.2014 | Original Article

A role for anterior thalamic nuclei in contextual fear memory

verfasst von: A. Marchand, A. Faugère, E. Coutureau, M. Wolff

Erschienen in: Brain Structure and Function | Ausgabe 5/2014

Einloggen, um Zugang zu erhalten

Abstract

Understanding the neural processes that govern the attribution of a predictive value to environmental stimuli is a major issue in behavioural neuroscience. The main strategy to explore this question has been the use of Pavlovian fear conditioning paradigms. While a majority of studies have focussed on the specific role of the hippocampus and amygdala in contextual versus cued fear, very few studies examined the potential role of subcortical limbic areas. Among those, the anterior thalamic nuclei (ATN) connect to both the hippocampus and the amygdala and also to the cingulate region which is known to support fear-related activity. Here, we show that rats sustaining ATN lesions exhibit a specific impairment following context but not tone conditioning. ATN lesions slowed down acquisition without preventing normal freezing behaviour when rats were reexposed to the conditioning context 24 h later. However, ATN rats exhibited poor retrieval of contextual but not cued fear when assessed 3 weeks after conditioning. In addition, extinction was faster in ATN rats and spontaneous recovery of contextual fear was impaired by the lesions. These deficits indicate that contextual fear memories established in the absence of the ATN are not robust. Collectively, these findings support an involvement of the ATN in the circuits underlying contextual fear memory.
Literatur
Zurück zum Zitat 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(1–2):189–198PubMedCrossRef 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(1–2):189–198PubMedCrossRef
Zurück zum Zitat Aggleton JP, Poirier GL, Aggleton HS, Vann SD, Pearce JM (2009) Lesions of the fornix and anterior thalamic nuclei dissociate different aspects of hippocampal-dependent spatial learning: implications for the neural basis of scene learning. Behav Neurosci 123(3):504–519. doi:10.1037/a0015404 PubMedCrossRef Aggleton JP, Poirier GL, Aggleton HS, Vann SD, Pearce JM (2009) Lesions of the fornix and anterior thalamic nuclei dissociate different aspects of hippocampal-dependent spatial learning: implications for the neural basis of scene learning. Behav Neurosci 123(3):504–519. doi:10.​1037/​a0015404 PubMedCrossRef
Zurück zum Zitat Aggleton JP, Amin E, Jenkins TA, Pearce JM, Robinson J (2011) Lesions in the anterior thalamic nuclei of rats do not disrupt acquisition of stimulus sequence learning. Q J Exp Psychol (Hove) 64(1):65–73. doi:10.1080/17470218).2010.495407 CrossRef Aggleton JP, Amin E, Jenkins TA, Pearce JM, Robinson J (2011) Lesions in the anterior thalamic nuclei of rats do not disrupt acquisition of stimulus sequence learning. Q J Exp Psychol (Hove) 64(1):65–73. doi:10.​1080/​17470218).​2010.​495407 CrossRef
Zurück zum Zitat Amin E, Wright N, Poirier GL, Thomas KL, Erichsen JT, Aggleton JP (2010) Selective lamina dysregulation in granular retrosplenial cortex (area 29) after anterior thalamic lesions: an in situ hybridization and trans-neuronal tracing study in rats. Neuroscience 169(3):1255–1267. doi:10.1016/j.neuroscience.2010.05.055 PubMedCrossRef Amin E, Wright N, Poirier GL, Thomas KL, Erichsen JT, Aggleton JP (2010) Selective lamina dysregulation in granular retrosplenial cortex (area 29) after anterior thalamic lesions: an in situ hybridization and trans-neuronal tracing study in rats. Neuroscience 169(3):1255–1267. doi:10.​1016/​j.​neuroscience.​2010.​05.​055 PubMedCrossRef
Zurück zum Zitat Anagnostaras SG, Maren S, Fanselow MS (1999) Temporally graded retrograde amnesia of contextual fear after hippocampal damage in rats: within-subjects examination. J Neurosci 19(3):1106–1114PubMed Anagnostaras SG, Maren S, Fanselow MS (1999) Temporally graded retrograde amnesia of contextual fear after hippocampal damage in rats: within-subjects examination. J Neurosci 19(3):1106–1114PubMed
Zurück zum Zitat Barbelivien A, Herbeaux K, Oberling P, Kelche C, Galani R, Majchrzak M (2006) Environmental enrichment increases responding to contextual cues but decreases overall conditioned fear in the rat. Behav Brain Res 169(2):231–238. doi:10.1016/j.bbr.2006.01.012 PubMedCrossRef Barbelivien A, Herbeaux K, Oberling P, Kelche C, Galani R, Majchrzak M (2006) Environmental enrichment increases responding to contextual cues but decreases overall conditioned fear in the rat. Behav Brain Res 169(2):231–238. doi:10.​1016/​j.​bbr.​2006.​01.​012 PubMedCrossRef
Zurück zum Zitat Celerier A, Ognard R, Decorte L, Beracochea D (2000) Deficits of spatial and non-spatial memory and of auditory fear conditioning following anterior thalamic lesions in mice: comparison with chronic alcohol consumption. Eur J Neurosci 12(7):2575–2584. pii:ejn115PubMedCrossRef Celerier A, Ognard R, Decorte L, Beracochea D (2000) Deficits of spatial and non-spatial memory and of auditory fear conditioning following anterior thalamic lesions in mice: comparison with chronic alcohol consumption. Eur J Neurosci 12(7):2575–2584. pii:ejn115PubMedCrossRef
Zurück zum Zitat Cho YH, Friedman E, Silva AJ (1999) Ibotenate lesions of the hippocampus impair spatial learning but not contextual fear conditioning in mice. Behav Brain Res 98(1):77–87. pii:S0166432898000540PubMedCrossRef Cho YH, Friedman E, Silva AJ (1999) Ibotenate lesions of the hippocampus impair spatial learning but not contextual fear conditioning in mice. Behav Brain Res 98(1):77–87. pii:S0166432898000540PubMedCrossRef
Zurück zum Zitat 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: interaction with environmental conditions. Hippocampus 23(5):392–404. doi:10.1002/hipo.22098 PubMedCrossRef 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: interaction with environmental conditions. Hippocampus 23(5):392–404. doi:10.​1002/​hipo.​22098 PubMedCrossRef
Zurück zum Zitat Esclassan F, Coutureau E, Di Scala G, Marchand AR (2009b) Differential contribution of dorsal and ventral hippocampus to trace and delay fear conditioning. Hippocampus 19(1):33–44. doi:10.1002/hipo.20473 PubMedCrossRef Esclassan F, Coutureau E, Di Scala G, Marchand AR (2009b) Differential contribution of dorsal and ventral hippocampus to trace and delay fear conditioning. Hippocampus 19(1):33–44. doi:10.​1002/​hipo.​20473 PubMedCrossRef
Zurück zum Zitat Frankland PW, Cestari V, Filipkowski RK, McDonald RJ, Silva AJ (1998) The dorsal hippocampus is essential for context discrimination but not for contextual conditioning. Behav Neurosci 112(4):863–874PubMedCrossRef Frankland PW, Cestari V, Filipkowski RK, McDonald RJ, Silva AJ (1998) The dorsal hippocampus is essential for context discrimination but not for contextual conditioning. Behav Neurosci 112(4):863–874PubMedCrossRef
Zurück zum Zitat Gibb SJ, Wolff M, Dalrymple-Alford JC (2006) Odour-place paired-associate learning and limbic thalamus: comparison of anterior, lateral and medial thalamic lesions. Behav Brain Res 172(1):155–168PubMedCrossRef Gibb SJ, Wolff M, Dalrymple-Alford JC (2006) Odour-place paired-associate learning and limbic thalamus: comparison of anterior, lateral and medial thalamic lesions. Behav Brain Res 172(1):155–168PubMedCrossRef
Zurück zum Zitat Hall J, Thomas KL, Everitt BJ (2001) Cellular imaging of zif268 expression in the hippocampus and amygdala during contextual and cued fear memory retrieval: selective activation of hippocampal CA1 neurons during the recall of contextual memories. J Neurosci 21(6):2186–2193. pii:21/6/2186PubMed Hall J, Thomas KL, Everitt BJ (2001) Cellular imaging of zif268 expression in the hippocampus and amygdala during contextual and cued fear memory retrieval: selective activation of hippocampal CA1 neurons during the recall of contextual memories. J Neurosci 21(6):2186–2193. pii:21/6/2186PubMed
Zurück zum Zitat Jenkins TA, Dias R, Amin E, Aggleton JP (2002a) Changes in Fos expression in the rat brain after unilateral lesions of the anterior thalamic nuclei. Eur J Neurosci 16(8):1425–1432. pii:2211PubMedCrossRef Jenkins TA, Dias R, Amin E, Aggleton JP (2002a) Changes in Fos expression in the rat brain after unilateral lesions of the anterior thalamic nuclei. Eur J Neurosci 16(8):1425–1432. pii:2211PubMedCrossRef
Zurück zum Zitat Jenkins TA, Dias R, Amin E, Brown MW, Aggleton JP (2002b) Fos imaging reveals that lesions of the anterior thalamic nuclei produce widespread limbic hypoactivity in rats. J Neurosci 22(12):5230–5238. pii:22/12/5230PubMed Jenkins TA, Dias R, Amin E, Brown MW, Aggleton JP (2002b) Fos imaging reveals that lesions of the anterior thalamic nuclei produce widespread limbic hypoactivity in rats. J Neurosci 22(12):5230–5238. pii:22/12/5230PubMed
Zurück zum Zitat Loukavenko EA, Ottley MC, Moran JP, Wolff M, Dalrymple-Alford JC (2007) Towards therapy to relieve memory impairment after anterior thalamic lesions: improved spatial working memory after immediate and delayed postoperative enrichment. Eur J Neurosci 26(11):3267–3276. doi:10.1111/j.1460-9568.2007.05879.x PubMedCrossRef Loukavenko EA, Ottley MC, Moran JP, Wolff M, Dalrymple-Alford JC (2007) Towards therapy to relieve memory impairment after anterior thalamic lesions: improved spatial working memory after immediate and delayed postoperative enrichment. Eur J Neurosci 26(11):3267–3276. doi:10.​1111/​j.​1460-9568.​2007.​05879.​x PubMedCrossRef
Zurück zum Zitat Marchand AR, Luck D, DiScala G (2003) Evaluation of an improved automated analysis of freezing behaviour in rats and its use in trace fear conditioning. J Neurosci Methods 126(2):145–153. pii:S0165027003000761PubMedCrossRef Marchand AR, Luck D, DiScala G (2003) Evaluation of an improved automated analysis of freezing behaviour in rats and its use in trace fear conditioning. J Neurosci Methods 126(2):145–153. pii:S0165027003000761PubMedCrossRef
Zurück zum Zitat Maren S, Fanselow MS (1997) Electrolytic lesions of the fimbria/fornix, dorsal hippocampus, or entorhinal cortex produce anterograde deficits in contextual fear conditioning in rats. Neurobiol Learn Mem 67(2):142–149. doi:10.1006/nlme.1996.3752 PubMedCrossRef Maren S, Fanselow MS (1997) Electrolytic lesions of the fimbria/fornix, dorsal hippocampus, or entorhinal cortex produce anterograde deficits in contextual fear conditioning in rats. Neurobiol Learn Mem 67(2):142–149. doi:10.​1006/​nlme.​1996.​3752 PubMedCrossRef
Zurück zum Zitat Maren S, Aharonov G, Fanselow MS (1997) Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav Brain Res 88(2):261–274. pii:S0166432897000880PubMedCrossRef Maren S, Aharonov G, Fanselow MS (1997) Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav Brain Res 88(2):261–274. pii:S0166432897000880PubMedCrossRef
Zurück zum Zitat Maren S, Anagnostaras SG, Fanselow MS (1998) The startled seahorse: is the hippocampus necessary for contextual fear conditioning? Trends Cogn Sci 2(2):39–42. pii:S1364-6613(98)01123-1PubMedCrossRef Maren S, Anagnostaras SG, Fanselow MS (1998) The startled seahorse: is the hippocampus necessary for contextual fear conditioning? Trends Cogn Sci 2(2):39–42. pii:S1364-6613(98)01123-1PubMedCrossRef
Zurück zum Zitat McNish KA, Gewirtz JC, Davis M (1997) Evidence of contextual fear after lesions of the hippocampus: a disruption of freezing but not fear-potentiated startle. J Neurosci 17(23):9353–9360PubMed McNish KA, Gewirtz JC, Davis M (1997) Evidence of contextual fear after lesions of the hippocampus: a disruption of freezing but not fear-potentiated startle. J Neurosci 17(23):9353–9360PubMed
Zurück zum Zitat McNish KA, Gewirtz JC, Davis M (1998) Have we taken the hippocampus out of context?-Reply. Trends Cogn Sci 2(2):42–43. pii:S1364-6613(98)01124-3PubMedCrossRef McNish KA, Gewirtz JC, Davis M (1998) Have we taken the hippocampus out of context?-Reply. Trends Cogn Sci 2(2):42–43. pii:S1364-6613(98)01124-3PubMedCrossRef
Zurück zum Zitat McNish KA, Gewirtz JC, Davis M (2000) Disruption of contextual freezing, but not contextual blocking of fear-potentiated startle, after lesions of the dorsal hippocampus. Behav Neurosci 114(1):64–76PubMedCrossRef McNish KA, Gewirtz JC, Davis M (2000) Disruption of contextual freezing, but not contextual blocking of fear-potentiated startle, after lesions of the dorsal hippocampus. Behav Neurosci 114(1):64–76PubMedCrossRef
Zurück zum Zitat Rescorla RA, Wagner AR (1972) A theory of Pavlovian conditioning; variations in the effectiveness of reinforcement and non reinforcement. In: A.H. Black WFP (ed) Classical conditioning II: current research and theory. Appleton-Century-Crofts, New-York, pp 64–99 Rescorla RA, Wagner AR (1972) A theory of Pavlovian conditioning; variations in the effectiveness of reinforcement and non reinforcement. In: A.H. Black WFP (ed) Classical conditioning II: current research and theory. Appleton-Century-Crofts, New-York, pp 64–99
Zurück zum Zitat Trifilieff P, Calandreau L, Herry C, Mons N, Micheau J (2007) Biphasic ERK1/2 activation in both the hippocampus and amygdala may reveal a system consolidation of contextual fear memory. Neurobiol Learn Mem 88(4):424–434. doi:10.1016/j.nlm.2007.05.004 PubMedCrossRef Trifilieff P, Calandreau L, Herry C, Mons N, Micheau J (2007) Biphasic ERK1/2 activation in both the hippocampus and amygdala may reveal a system consolidation of contextual fear memory. Neurobiol Learn Mem 88(4):424–434. doi:10.​1016/​j.​nlm.​2007.​05.​004 PubMedCrossRef
Zurück zum Zitat Van Groen T, Vogt BA, Wyss JM (1993) Interconnections between the thalamus and retrosplenial cortex in the rodent brain. In: Vogt BA, M. G (eds) Neurobiology of Cingulate Cortex and Limbic Thalamus. Birkhäuser, Boston, pp 123–150 Van Groen T, Vogt BA, Wyss JM (1993) Interconnections between the thalamus and retrosplenial cortex in the rodent brain. In: Vogt BA, M. G (eds) Neurobiology of Cingulate Cortex and Limbic Thalamus. Birkhäuser, Boston, pp 123–150
Zurück zum Zitat van Groen T, Kadish I, Wyss JM (1999) Efferent connections of the anteromedial nucleus of the thalamus of the rat. Brain Res Brain Res Rev 30(1):1–26. pii:S0165017399000065PubMedCrossRef van Groen T, Kadish I, Wyss JM (1999) Efferent connections of the anteromedial nucleus of the thalamus of the rat. Brain Res Brain Res Rev 30(1):1–26. pii:S0165017399000065PubMedCrossRef
Zurück zum Zitat van Groen T, Kadish I, Michael Wyss J (2002) Role of the anterodorsal and anteroventral nuclei of the thalamus in spatial memory in the rat. Behav Brain Res 132(1):19–28. pii:S0165017399000065PubMedCrossRef van Groen T, Kadish I, Michael Wyss J (2002) Role of the anterodorsal and anteroventral nuclei of the thalamus in spatial memory in the rat. Behav Brain Res 132(1):19–28. pii:S0165017399000065PubMedCrossRef
Zurück zum Zitat Warburton EC, Baird AL, Aggleton JP (1997) Assessing the magnitude of the allocentric spatial deficit associated with complete loss of the anterior thalamic nuclei in rats. Behav Brain Res 87(2):223–232. pii:S0166-4328(97)02285-7PubMedCrossRef Warburton EC, Baird AL, Aggleton JP (1997) Assessing the magnitude of the allocentric spatial deficit associated with complete loss of the anterior thalamic nuclei in rats. Behav Brain Res 87(2):223–232. pii:S0166-4328(97)02285-7PubMedCrossRef
Zurück zum Zitat Warburton EC, Baird A, Morgan A, Muir JL, Aggleton JP (2001) The conjoint importance of the hippocampus and anterior thalamic nuclei for allocentric spatial learning: evidence from a disconnection study in the rat. J Neurosci 21(18):7323–7330. pii:21/18/7323PubMed Warburton EC, Baird A, Morgan A, Muir JL, Aggleton JP (2001) The conjoint importance of the hippocampus and anterior thalamic nuclei for allocentric spatial learning: evidence from a disconnection study in the rat. J Neurosci 21(18):7323–7330. pii:21/18/7323PubMed
Zurück zum Zitat Ward-Robinson J, Wilton LA, Muir JL, Honey RC, Vann SD, Aggleton JP (2002) Sensory preconditioning in rats with lesions of the anterior thalamic nuclei: evidence for intact nonspatial ‘relational’ processing. Behav Brain Res 133(2):125–133. pii:S016643280100465XPubMedCrossRef Ward-Robinson J, Wilton LA, Muir JL, Honey RC, Vann SD, Aggleton JP (2002) Sensory preconditioning in rats with lesions of the anterior thalamic nuclei: evidence for intact nonspatial ‘relational’ processing. Behav Brain Res 133(2):125–133. pii:S016643280100465XPubMedCrossRef
Zurück zum Zitat 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(11):2907–2913PubMedCrossRef 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(11):2907–2913PubMedCrossRef
Zurück zum Zitat Wolff M, Gibb SJ, Cassel JC, Dalrymple-Alford JC (2008a) Anterior but not intralaminar thalamic nuclei support allocentric spatial memory. Neurobiol Learn Mem 90(1):71–80PubMedCrossRef Wolff M, Gibb SJ, Cassel JC, Dalrymple-Alford JC (2008a) Anterior but not intralaminar thalamic nuclei support allocentric spatial memory. Neurobiol Learn Mem 90(1):71–80PubMedCrossRef
Zurück zum Zitat Wolff M, Loukavenko EA, Will BE, Dalrymple-Alford JC (2008b) The extended hippocampal-diencephalic memory system: enriched housing promotes recovery of the flexible use of spatial representations after anterior thalamic lesions. Hippocampus 18(10):996–1007. doi:10.1002/hipo.20457 PubMedCrossRef Wolff M, Loukavenko EA, Will BE, Dalrymple-Alford JC (2008b) The extended hippocampal-diencephalic memory system: enriched housing promotes recovery of the flexible use of spatial representations after anterior thalamic lesions. Hippocampus 18(10):996–1007. doi:10.​1002/​hipo.​20457 PubMedCrossRef
Zurück zum Zitat Wright NF, Erichsen JT, Vann SD, O’Mara SM, Aggleton JP (2010) Parallel but separate inputs from limbic cortices to the mammillary bodies and anterior thalamic nuclei in the rat. J Comp Neurol 518(12):2334–2354. doi:10.1002/cne.22336 PubMedCrossRef Wright NF, Erichsen JT, Vann SD, O’Mara SM, Aggleton JP (2010) Parallel but separate inputs from limbic cortices to the mammillary bodies and anterior thalamic nuclei in the rat. J Comp Neurol 518(12):2334–2354. doi:10.​1002/​cne.​22336 PubMedCrossRef
Metadaten
Titel
A role for anterior thalamic nuclei in contextual fear memory
verfasst von
A. Marchand
A. Faugère
E. Coutureau
M. Wolff
Publikationsdatum
01.09.2014
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 5/2014
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-013-0586-7

Weitere Artikel der Ausgabe 5/2014

Brain Structure and Function 5/2014 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Niedriger diastolischer Blutdruck erhöht Risiko für schwere kardiovaskuläre Komplikationen

25.04.2024 Hypotonie Nachrichten

Wenn unter einer medikamentösen Hochdrucktherapie der diastolische Blutdruck in den Keller geht, steigt das Risiko für schwere kardiovaskuläre Ereignisse: Darauf deutet eine Sekundäranalyse der SPRINT-Studie hin.

Frühe Alzheimertherapie lohnt sich

25.04.2024 AAN-Jahrestagung 2024 Nachrichten

Ist die Tau-Last noch gering, scheint der Vorteil von Lecanemab besonders groß zu sein. Und beginnen Erkrankte verzögert mit der Behandlung, erreichen sie nicht mehr die kognitive Leistung wie bei einem früheren Start. Darauf deuten neue Analysen der Phase-3-Studie Clarity AD.

Viel Bewegung in der Parkinsonforschung

25.04.2024 Parkinson-Krankheit Nachrichten

Neue arznei- und zellbasierte Ansätze, Frühdiagnose mit Bewegungssensoren, Rückenmarkstimulation gegen Gehblockaden – in der Parkinsonforschung tut sich einiges. Auf dem Deutschen Parkinsonkongress ging es auch viel um technische Innovationen.

Demenzkranke durch Antipsychotika vielfach gefährdet

23.04.2024 Demenz Nachrichten

Wenn Demenzkranke aufgrund von Symptomen wie Agitation oder Aggressivität mit Antipsychotika behandelt werden, sind damit offenbar noch mehr Risiken verbunden als bislang angenommen.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.