Functional heterogeneity of the limbic thalamus: From hippocampal to cortical functions

Today, the idea that the integrity of the limbic thalamus is necessary for normal memory functions is well established. However, if the study of thalamic patients emphasized the anterior and the mediodorsal thalamus as the critical thalamic loci supporting cognitive functions, clinical studies have so far failed to attribute a specific role to each of these regions. In view of these difficulties, we review here the experimental data conducted in rodents harboring specific lesions of each thalamic region. These data clearly indicate a major functional dissociation within the limbic thalamus. The anterior thalamus provides critical support for hippocampal functions due to its cardinal location in the Papez circuit, while the mediodorsal thalamus may signal relevant information in a circuit encompassing the basolateral amygdala and the prefrontal cortex. Interestingly, while clinical studies have suggested that diencephalic pathologies may disconnect the medial temporal lobe from the cortex, experimental studies conducted in rodent show how this may differently affect distinct temporo-thalamo-cortical circuits, sharing the same general organization but supporting dissociable functions.

[1]  C. Caltagirone,et al.  Vascular thalamic amnesia: A reappraisal , 2011, Neuropsychologia.

[2]  S. Floresco,et al.  Cerebral Cortex doi:10.1093/cercor/bhl073 Thalamic--Prefrontal Cortical--Ventral Striatal Circuitry Mediates Dissociable Components of Strategy Set Shifting , 2006 .

[3]  S. Sherman,et al.  Thalamic relays and cortical functioning. , 2005, Progress in brain research.

[4]  Seralynne D. Vann,et al.  How do mammillary body inputs contribute to anterior thalamic function? , 2015, Neuroscience & Biobehavioral Reviews.

[5]  M. E. Corcoran,et al.  Thalamic and hippocampal mechanisms in spatial navigation: A dissociation between brain mechanisms for learning how versus learning where to navigate , 2006, Behavioural Brain Research.

[6]  Julie R. Dumont,et al.  Fornix and retrosplenial contribution to a hippocampo-thalamic circuit underlying conditional learning , 2010, Behavioural Brain Research.

[7]  Menno P. Witter,et al.  Neurotoxic lesions of the thalamic reuniens or mediodorsal nucleus in rats affect non-mnemonic aspects of watermaze learning , 2009, Brain Structure and Function.

[8]  E. Coutureau,et al.  Goal-directed responding is sensitive to lesions to the prelimbic cortex or basolateral nucleus of the amygdala but not to their disconnection. , 2009, Behavioral neuroscience.

[9]  J. Aggleton Multiple anatomical systems embedded within the primate medial temporal lobe: Implications for hippocampal function , 2012, Neuroscience & Biobehavioral Reviews.

[10]  David M. Smith,et al.  Hippocampal place cells, context, and episodic memory , 2006, Hippocampus.

[11]  J. Mitrofanis,et al.  Organisation of the amygdalo-thalamic pathways in rats , 2000, Anatomy and Embryology.

[12]  Benjamin J Clark,et al.  Head direction cell activity in the anterodorsal thalamus requires intact supragenual nuclei. , 2012, Journal of neurophysiology.

[13]  M. A. Peinado-Manzano,et al.  Retrograde amnesia in rats with dorsomedial thalamic damage , 1996, Behavioural Brain Research.

[14]  John P. Aggleton,et al.  The Conjoint Importance of the Hippocampus and Anterior Thalamic Nuclei for Allocentric Spatial Learning: Evidence from a Disconnection Study in the Rat , 2001, The Journal of Neuroscience.

[15]  B. Balleine,et al.  The Effect of Lesions of the Basolateral Amygdala on Instrumental Conditioning , 2003, The Journal of Neuroscience.

[16]  John P. Aggleton,et al.  Interleaving brain systems for episodic and recognition memory , 2006, Trends in Cognitive Sciences.

[17]  A. Stevens,et al.  A comparison of temporal decay in place memory tasks in rats (Rattus norvegicus) with lesions affecting thalamus, frontal cortex, or the hippocampal system. , 1996, Behavioral neuroscience.

[18]  M. Kopelman,et al.  The Korsakoff syndrome: clinical aspects, psychology and treatment. , 2009, Alcohol and alcoholism.

[19]  John P Aggleton,et al.  Differential deficits in the Morris water maze following cytotoxic lesions of the anterior thalamus and fornix transection , 1998, Behavioural Brain Research.

[20]  J. Aggleton,et al.  Neurotoxic Lesions of the Dorsomedial Thalamus Impair the Acquisition But Not the Performance of Delayed Matching to Place by Rats: a Deficit in Shifting Response Rules , 1998, The Journal of Neuroscience.

[21]  G. Winocur The hippocampus and thalamus: Their roles in short- and long-term memory and the effects of interference , 1985, Behavioural Brain Research.

[22]  Seralynne D Vann,et al.  Dismantling the Papez circuit for memory in rats , 2013, eLife.

[23]  J. Pearce,et al.  Lesions in the anterior thalamic nuclei of rats do not disrupt acquisition of stimulus sequence learning , 2011, Quarterly journal of experimental psychology.

[24]  B. Balleine,et al.  Human and Rodent Homologies in Action Control: Corticostriatal Determinants of Goal-Directed and Habitual Action , 2010, Neuropsychopharmacology.

[25]  H. Shibata,et al.  Efferent projections from the anterior thalamic nuclei to the cingulate cortex in the rat , 1993, The Journal of comparative neurology.

[26]  M. Gabriel,et al.  Limbic thalamic, cingulate cortical and hippocampal neuronal correlates of discriminative approach learning in rabbits , 1996, Behavioural Brain Research.

[27]  Mathieu Wolff,et al.  The extended hippocampal‐diencephalic memory system: Enriched housing promotes recovery of the flexible use of spatial representations after anterior thalamic lesions , 2008, Hippocampus.

[28]  J. Dalrymple-Alford,et al.  Perirhinal cortex and anterior thalamic lesions: comparative effects on learning and memory. , 2003, Behavioral neuroscience.

[29]  T. Bussey,et al.  Effects of selective thalamic and prelimbic cortex lesions on two types of visual discrimination and reversal learning , 2001, The European journal of neuroscience.

[30]  Matthew L. Tullman,et al.  Lesions of the Tegmentomammillary Circuit in the Head Direction System Disrupt the Head Direction Signal in the Anterior Thalamus , 2007, The Journal of Neuroscience.

[31]  D. Béracochéa,et al.  Effects of anterior or dorsomedial thalamic ibotenic lesions on learning and memory in rats. , 1989, Behavioral and neural biology.

[32]  P. Goldman-Rakic Anatomical and functional circuits in prefrontal cortex of nonhuman primates. Relevance to epilepsy. , 1995, Advances in neurology.

[33]  Jeffrey S. Taube,et al.  Impaired Head Direction Cell Representation in the Anterodorsal Thalamus after Lesions of the Retrosplenial Cortex , 2010, The Journal of Neuroscience.

[34]  H. Eichenbaum A cortical–hippocampal system for declarative memory , 2000, Nature Reviews Neuroscience.

[35]  Inga Kadish,et al.  Role of the anterodorsal and anteroventral nuclei of the thalamus in spatial memory in the rat , 2002, Behavioural Brain Research.

[36]  C. Pickens A limited role for mediodorsal thalamus in devaluation tasks. , 2008, Behavioral neuroscience.

[37]  M. Gabriel,et al.  Cingulate cortical and anterior thalamic neuronal correlates of reversal learning in rabbits. , 1980, Journal of comparative and physiological psychology.

[38]  J. Aggleton,et al.  Assessing the magnitude of the allocentric spatial deficit associated with complete loss of the anterior thalamic nuclei in rats , 1997, Behavioural Brain Research.

[39]  W. Scoville,et al.  Loss of Recent Memory After Bilateral Hippocampal Lesions , 2000 .

[40]  J. Dalrymple-Alford,et al.  Odour–place paired-associate learning and limbic thalamus: Comparison of anterior, lateral and medial thalamic lesions , 2006, Behavioural Brain Research.

[41]  J. Aggleton,et al.  The effects of selective lesions within the anterior thalamic nuclei on spatial memory in the rat , 1996, Behavioural Brain Research.

[42]  G. Romani,et al.  Functional MRI study of diencephalic amnesia in Wernicke-Korsakoff syndrome. , 2005, Brain : a journal of neurology.

[43]  R. C. Honey,et al.  Sensory preconditioning in rats with lesions of the anterior thalamic nuclei: evidence for intact nonspatial ‘relational’ processing , 2002, Behavioural Brain Research.

[44]  G. Winocur Anterograde and retrograde amnesia in rats with dorsal hippocampal or dorsomedial thalamic lesions , 1990, Behavioural Brain Research.

[45]  John P Aggleton,et al.  Please Scroll down for Article the Quarterly Journal of Experimental Psychology Understanding Anterograde Amnesia: Disconnections and Hidden Lesions , 2022 .

[46]  T. Groen,et al.  The role of the laterodorsal nucleus of the thalamus in spatial learning and memory in the rat , 2002, Behavioural Brain Research.

[47]  R. Mair,et al.  Effects of thalamic and olfactory cortical lesions on continuous olfactory delayed nonmatching-to-sample and olfactory discrimination in rats (Rattus norvegicus). , 1998, Behavioral neuroscience.

[48]  L. Squire,et al.  The anatomy of amnesia: neurohistological analysis of three new cases. , 2006, Learning & memory.

[49]  Moriel Zelikowsky,et al.  Contextual Fear Memories Formed in the Absence of the Dorsal Hippocampus Decay Across Time , 2012, The Journal of Neuroscience.

[50]  M. Gabriel,et al.  Neural substrates of discriminative avoidance learning and classical eyeblink conditioning in rabbits: a double dissociation , 1996, Behavioural Brain Research.

[51]  Anna S. Mitchell,et al.  Lateral and anterior thalamic lesions impair independent memory systems. , 2006, Learning & memory.

[52]  J. Taube,et al.  Behavioral/systems/cognitive Hippocampal Place Cell Instability after Lesions of the Head Direction Cell Network , 2022 .

[53]  A. Lozano,et al.  Anterior thalamus deep brain stimulation at high current impairs memory in rats , 2010, Experimental Neurology.

[54]  M. Gabriel,et al.  Context-specific multi-site cingulate cortical, limbic thalamic, and hippocampal neuronal activity during concurrent discriminative approach and avoidance training in rabbits , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  M. Gabriel,et al.  Anterior thalamic lesions and neuronal activity in the cingulate and retrosplenial cortices during discriminative avoidance behavior in rabbits. , 1983, Behavioral neuroscience.

[56]  Seralynne D Vann,et al.  Do rats with retrosplenial cortex lesions lack direction? , 2008, The European journal of neuroscience.

[57]  B. Balleine,et al.  Differential Involvement of the Basolateral Amygdala and Mediodorsal Thalamus in Instrumental Action Selection , 2008, The Journal of Neuroscience.

[58]  David M. Smith,et al.  Hippocampal context processing is critical for interference free recall of odor memories in rats , 2012, Hippocampus.

[59]  M. Gabriel,et al.  Neuronal encoding of conditional stimulus duration in the cingulate cortex and the limbic thalamus of rabbits. , 1990, Behavioral neuroscience.

[60]  Anthony A Grace,et al.  Gating of Hippocampal-Evoked Activity in Prefrontal Cortical Neurons by Inputs from the Mediodorsal Thalamus and Ventral Tegmental Area , 2003, The Journal of Neuroscience.

[61]  R. Sutherland,et al.  The role of the fornix/fimbria and some related subcortical structures in place learning and memory , 1989, Behavioural Brain Research.

[62]  Raymond P. Kesner,et al.  The role of the hippocampus in memory for the temporal order of a sequence of odors. , 2002 .

[63]  J. Aggleton,et al.  eview hy do lesions in the rodent anterior thalamic nuclei cause such evere spatial deficits ? , 2015 .

[64]  H. Eichenbaum,et al.  The Hippocampus, Memory, and Place Cells Is It Spatial Memory or a Memory Space? , 1999, Neuron.

[65]  R. C. Honey,et al.  Loss of the thalamic nuclei for "head direction" impairs performance on spatial memory tasks in rats. , 2001, Behavioral neuroscience.

[66]  Sheri J. Y. Mizumori,et al.  Context Prediction Analysis and Episodic Memory , 2013, Front. Behav. Neurosci..

[67]  F. Chauveau,et al.  Effects of ibotenic acid lesions of the mediodorsal thalamus on memory: relationship with emotional processes in mice , 2005, Behavioural Brain Research.

[68]  A. McDonald Organization of amygdaloid projections to the mediodorsal thalamus and prefrontal cortex: A fluorescence retrograde transport study in the rat , 1987, The Journal of comparative neurology.

[69]  Hauke Bartsch,et al.  Postmortem examination of patient H.M.’s brain based on histological sectioning and digital 3D reconstruction , 2014, Nature Communications.

[70]  J. T. Erichsen,et al.  The anterior thalamus provides a subcortical circuit supporting memory and spatial navigation , 2013, Front. Syst. Neurosci..

[71]  J. Muir,et al.  Disconnecting hippocampal projections to the anterior thalamus produces deficits on tests of spatial memory in rats , 2000, The European journal of neuroscience.

[72]  Anna S. Mitchell,et al.  Dissociable memory effects after medial thalamus lesions in the rat , 2005, The European journal of neuroscience.

[73]  J. Aggleton,et al.  Selective disconnection of the hippocampal formation projections to the mammillary bodies produces only mild deficits on spatial memory tasks: Implications for fornix function , 2011, Hippocampus.

[74]  B. Balleine,et al.  Lesions of mediodorsal thalamus and anterior thalamic nuclei produce dissociable effects on instrumental conditioning in rats , 2003, The European journal of neuroscience.

[75]  Elizabeth K. Warrington,et al.  Amnesia: A disconnection syndrome? , 1982, Neuropsychologia.

[76]  J. Taube,et al.  Firing Properties of Head Direction Cells in the Rat Anterior Thalamic Nucleus: Dependence on Vestibular Input , 1997, The Journal of Neuroscience.

[77]  Dissociable effects of anterior and mediodorsal thalamic lesions on spatial goal-directed behavior , 2014, Brain Structure and Function.

[78]  M. W. Brown,et al.  Episodic memory, amnesia, and the hippocampal–anterior thalamic axis , 1999, Behavioral and Brain Sciences.

[79]  T. Bussey,et al.  Triple dissociation of anterior cingulate, posterior cingulate, and medial frontal cortices on visual discrimination tasks using a touchscreen testing procedure for the rat. , 1997, Behavioral neuroscience.

[80]  J. Aggleton,et al.  Lack of effect of dorsomedial thalamic lesions on automated tests of spatial memory in the rat , 1993, Behavioural Brain Research.

[81]  B. Hampstead,et al.  Thalamic Contributions to Anterograde, Retrograde, and Implicit Memory: A Case Study , 2009, The Clinical neuropsychologist.

[82]  S. Killcross,et al.  Coordination of actions and habits in the medial prefrontal cortex of rats. , 2003, Cerebral cortex.

[83]  Stan B. Floresco,et al.  Thalamic–Cortical–Striatal Circuitry Subserves Working Memory during Delayed Responding on a Radial Arm Maze , 1999, The Journal of Neuroscience.

[84]  Feinberg Jf The Wernicke-Korsakoff syndrome. , 1980 .

[85]  H. Groenewegen Organization of the afferent connections of the mediodorsal thalamic nucleus in the rat, related to the mediodorsal-prefrontal topography , 1988, Neuroscience.

[86]  D. Mumby,et al.  Mediodorsal thalamic lesions and object recognition in rats , 1993, Psychobiology.

[87]  Hideshi Shibata,et al.  Organization of anterior cingulate and frontal cortical projections to the anterior and laterodorsal thalamic nuclei in the rat , 2005, Brain Research.

[88]  L. Means,et al.  Effects of dorsomedial thalamic lesions on spatial discrimination reversal in the rat , 1975, Physiology & Behavior.

[89]  G. Pergola,et al.  Associative Learning Beyond the Medial Temporal Lobe: Many Actors on the Memory Stage , 2013, Front. Behav. Neurosci..

[90]  S. Funahashi,et al.  Thalamic mediodorsal nucleus and working memory , 2012, Neuroscience & Biobehavioral Reviews.

[91]  J. Dalrymple-Alford,et al.  Anterior but not intralaminar thalamic nuclei support allocentric spatial memory , 2008, Neurobiology of Learning and Memory.

[92]  A role for anterior thalamic nuclei in contextual fear memory , 2014, Brain Structure and Function.

[93]  D. Béracochéa,et al.  Effects of mammillary bodies and mediodorsal thalamic lesions on the acquisition and retention of a learning set in mice: paradoxical effect of the intersession interval , 1995, Behavioural Brain Research.

[94]  John P. Aggleton,et al.  Understanding retrosplenial amnesia: Insights from animal studies , 2010, Neuropsychologia.

[95]  Lesions of the anterior thalamic nuclei and intralaminar thalamic nuclei: place and visual discrimination learning in the water maze , 2013, Brain Structure and Function.

[96]  J. Aggleton,et al.  Medial dorsal thalamic lesions and working memory in the rat. , 1991, Behavioral and neural biology.

[97]  J. Kril,et al.  Neuroanatomy and Neuropathology Associated with Korsakoff’s Syndrome , 2012, Neuropsychology Review.

[98]  Ryan D Ward,et al.  Mediodorsal Thalamus Hypofunction Impairs Flexible Goal-Directed Behavior , 2015, Biological Psychiatry.

[99]  C. Barry,et al.  Neural Mechanisms of Self-Location , 2014, Current Biology.

[100]  E. Coutureau,et al.  Transient role of the rat prelimbic cortex in goal‐directed behaviour , 2009, The European journal of neuroscience.

[101]  Laura A. Bradfield,et al.  The role of the anterior, mediodorsal, and parafascicular thalamus in instrumental conditioning , 2013, Front. Syst. Neurosci..

[102]  J. Kril,et al.  Degeneration of anterior thalamic nuclei differentiates alcoholics with amnesia. , 2000, Brain : a journal of neurology.

[103]  J. Tigner,et al.  The effects of dorsomedial thalamic lesions on learning, reversal, and alternation behavior in the rat. , 1974, Physiology & behavior.

[104]  M. Gabriel,et al.  Hippocampal control of cingulate cortical and anterior thalamic information processing during learning in rabbits , 2004, Experimental Brain Research.

[105]  M. Gabriel,et al.  Unit activity in cingulate cortex and anteroventral thalamus of the rabbit during differential conditioning and reversal. , 1977, Journal of comparative and physiological psychology.

[106]  E. Murray,et al.  Functional Interaction of Medial Mediodorsal Thalamic Nucleus But Not Nucleus Accumbens with Amygdala and Orbital Prefrontal Cortex Is Essential for Adaptive Response Selection after Reinforcer Devaluation , 2010, The Journal of Neuroscience.

[107]  Both anteromedial and anteroventral thalamic lesions impair radial-maze learning in rats. , 1996 .

[108]  Seralynne D Vann,et al.  Lesions of the fornix and anterior thalamic nuclei dissociate different aspects of hippocampal-dependent spatial learning: implications for the neural basis of scene learning. , 2009, Behavioral neuroscience.

[109]  P. Best,et al.  Mediodorsal thalamic lesions impair “Reference” and “working” memory in rats , 1990, Physiology & Behavior.

[110]  B. Balleine,et al.  Goal-directed instrumental action: contingency and incentive learning and their cortical substrates , 1998, Neuropharmacology.

[111]  Jean-Christophe Cassel,et al.  The Intralaminar Thalamic Nuclei Contribute to Remote Spatial Memory , 2009, The Journal of Neuroscience.

[112]  B. Cosquer,et al.  The Ventral Midline Thalamus (Reuniens and Rhomboid Nuclei) Contributes to the Persistence of Spatial Memory in Rats , 2012, The Journal of Neuroscience.

[113]  N. Burgess,et al.  The hippocampus and memory: insights from spatial processing , 2008, Nature Reviews Neuroscience.

[114]  J. Taube The head direction signal: origins and sensory-motor integration. , 2007, Annual review of neuroscience.

[115]  B. Vogt,et al.  Interconnections Between the Thalamus and Retrosplenial Cortex in the Rodent Brain , 1993 .

[116]  Paul Leonard Gabbott,et al.  Prefrontal cortex in the rat: Projections to subcortical autonomic, motor, and limbic centers , 2005, The Journal of comparative neurology.

[117]  J. Knierim,et al.  Coupling between place cells and head direction cells during relative translations and rotations of distal landmarks , 2004, Experimental Brain Research.

[118]  J. Aggleton Looking beyond the hippocampus: old and new neurological targets for understanding memory disorders , 2014, Proceedings of the Royal Society B: Biological Sciences.

[119]  M. Gabriel,et al.  Cingulate cortical and anterior thalamic neuronal correlates of the overtraining reversal effect in rabbits , 1982, Behavioural Brain Research.

[120]  Papez Jw A proposed mechanism of emotion. 1937. , 1995 .

[121]  Jean Delay,et al.  Le Syndrome de Korsakoff , 1969 .

[122]  H. Eichenbaum,et al.  Critical role of the hippocampus in memory for sequences of events , 2002, Nature Neuroscience.

[123]  Seralynne D Vann,et al.  Dysgranular retrosplenial cortex lesions in rats disrupt cross-modal , 2014 .

[124]  E. Coutureau,et al.  A role for anterior thalamic nuclei in affective cognition: Interaction with environmental conditions , 2013, Hippocampus.

[125]  J. Aggleton,et al.  An examination of the spatial working memory deficit following neurotoxic medial dorsal thalamic lesions in rats , 1998, Behavioural Brain Research.

[126]  R. Mair,et al.  Lesions of specific and nonspecific thalamic nuclei affect prefrontal cortex-dependent aspects of spatial working memory. , 2005, Behavioral neuroscience.

[127]  B. Balleine,et al.  Parallel incentive processing: an integrated view of amygdala function , 2006, Trends in Neurosciences.

[128]  Mathieu Wolff,et al.  Beyond Spatial Memory: The Anterior Thalamus and Memory for the Temporal Order of a Sequence of Odor Cues , 2006, The Journal of Neuroscience.

[129]  Jeffrey S. Taube,et al.  Path integration: how the head direction signal maintains and corrects spatial orientation , 2012, Nature Neuroscience.

[130]  J. Dalrymple-Alford,et al.  Towards therapy to relieve memory impairment after anterior thalamic lesions: improved spatial working memory after immediate and delayed postoperative enrichment , 2007, The European journal of neuroscience.

[131]  W. Abraham,et al.  Effects of thalamic lesions on repeated relearning of a spatial working memory task , 2014, Behavioural Brain Research.

[132]  R. Mair,et al.  Thalamic amnesia reconsidered: excitotoxic lesions of the intralaminar nuclei, but not the mediodorsal nucleus, disrupt place delayed matching-to-sample performance in rats (Rattus norvegicus). , 1998, Behavioral neuroscience.

[133]  Anna S. Mitchell,et al.  What does the mediodorsal thalamus do? , 2013, Front. Syst. Neurosci..

[134]  J. Delacour,et al.  Selective fimbria and thalamic lesions differentially impair forms of working memory in rats. , 1991, Behavioral and neural biology.

[135]  S. Mizumori,et al.  Reversible inactivation of the lateral dorsal thalamus disrupts hippocampal place representation and impairs spatial learning , 1994, Brain Research.

[136]  David M. Smith,et al.  The anterior thalamus is critical for overcoming interference in a context-dependent odor discrimination task. , 2012, Behavioral neuroscience.

[137]  J. Aggleton,et al.  The rat retrosplenial cortex is required when visual cues are used flexibly to determine location , 2014, Behavioural Brain Research.

[138]  Michael Petrides,et al.  Spatial conditional associative learning: effects of thalamo-hippocampal disconnection in rats , 2004, Neuroreport.

[139]  Adam M. P. Miller,et al.  Cues, context, and long-term memory: the role of the retrosplenial cortex in spatial cognition , 2014, Front. Hum. Neurosci..

[140]  J. Aggleton,et al.  The medial dorsal thalamic nucleus and the medial prefrontal cortex of the rat function together to support associative recognition and recency but not item recognition , 2012, Learning & memory.

[141]  J. Muir,et al.  Does pretraining spare the spatial deficit associated with anterior thalamic damage in rats? , 1999, Behavioral neuroscience.

[142]  Ryan D Ward,et al.  Inhibition of Mediodorsal Thalamus Disrupts Thalamofrontal Connectivity and Cognition , 2013, Neuron.

[143]  B. Bontempi,et al.  Reduced cytochrome oxidase activity in the retrosplenial cortex after lesions to the anterior thalamic nuclei , 2013, Behavioural Brain Research.

[144]  R. Sutherland,et al.  Dissociation of the contributions of the prefrontal cortex and dorsomedial thalamic nucleus to spatially guided behavior in the rat , 1982, Behavioural Brain Research.

[145]  M. A. Peinado-Manzano,et al.  The role of different nuclei of the thalamus in processing episodic information , 1991, Behavioural Brain Research.

[146]  J. Taube,et al.  Head direction cells and episodic spatial information in rats without a hippocampus. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[147]  B. Balleine,et al.  Double Dissociation of Basolateral and Central Amygdala Lesions on the General and Outcome-Specific Forms of Pavlovian-Instrumental Transfer , 2005, The Journal of Neuroscience.

[148]  John P. Aggleton,et al.  Effects of selective granular retrosplenial cortex lesions on spatial working memory in rats , 2010, Behavioural Brain Research.

[149]  Shintaro Funahashi,et al.  Thalamic mediodorsal nucleus and its participation in spatial working memory processes: comparison with the prefrontal cortex , 2013, Front. Syst. Neurosci..

[150]  T. Singer,et al.  The neural basis of empathy. , 2012, Annual review of neuroscience.

[151]  P. Best,et al.  Response biases do not underlie the radial maze deficit in rats with mediodorsal thalamus lesions. , 1990, Behavioral and neural biology.

[152]  R. Vertes,et al.  The reuniens and rhomboid nuclei: Neuroanatomy, electrophysiological characteristics and behavioral implications , 2013, Progress in Neurobiology.

[153]  H. Shibata Direct projections from the anterior thalamic nuclei to the retrohippocampal region in the rat , 1993, The Journal of comparative neurology.

[154]  S. Vann Gudden's ventral tegmental nucleus is vital for memory: re-evaluating diencephalic inputs for amnesia. , 2009, Brain : a journal of neurology.

[155]  M. Gabriel,et al.  Anterior thalamic discriminative neuronal responses enhanced during learning in rabbits with subicular and cingulate cortical lesions , 1986, Brain Research.

[156]  J. Pinel,et al.  Rhinal cortex, but not medial thalamic, lesions cause retrograde amnesia for objects in rats. , 1999, Neuroreport.

[157]  J. Taube Head direction cells recorded in the anterior thalamic nuclei of freely moving rats , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[158]  T. Alexinsky Differential effect of thalamic and cortical lesions on memory systems in the rat , 2001, Behavioural Brain Research.

[159]  John M. Pearce,et al.  Hippocampal lesions disrupt navigation based on cognitive maps but not heading vectors , 1998, Nature.

[160]  H. Eichenbaum,et al.  Hippocampal representation in place learning , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.