Projection specificity in heterogeneous locus coeruleus cell populations: implications for learning and memory

Noradrenergic neurons in the locus coeruleus (LC) play a critical role in many functions including learning and memory. This relatively small population of cells sends widespread projections throughout the brain including to a number of regions such as the amygdala which is involved in emotional associative learning and the medial prefrontal cortex which is important for facilitating flexibility when learning rules change. LC noradrenergic cells participate in both of these functions, but it is not clear how this small population of neurons modulates these partially distinct processes. Here we review anatomical, behavioral, and electrophysiological studies to assess how LC noradrenergic neurons regulate these different aspects of learning and memory. Previous work has demonstrated that subpopulations of LC noradrenergic cells innervate specific brain regions suggesting heterogeneity of function in LC neurons. Furthermore, noradrenaline in mPFC and amygdala has distinct effects on emotional learning and cognitive flexibility. Finally, neural recording data show that LC neurons respond during associative learning and when previously learned task contingencies change. Together, these studies suggest a working model in which distinct and potentially opposing subsets of LC neurons modulate particular learning functions through restricted efferent connectivity with amygdala or mPFC. This type of model may provide a general framework for understanding other neuromodulatory systems, which also exhibit cell type heterogeneity and projection specificity.

[1]  B. Richmond,et al.  Relation of locus coeruleus neurons in monkeys to Pavlovian and operant behaviors. , 2009, Journal of neurophysiology.

[2]  Menek Goldstein,et al.  Activation of the locus coeruleus induced by selective stimulation of the ventral tegmental area , 1986, Brain Research.

[3]  O. Hardt,et al.  A single standard for memory: the case for reconsolidation , 2009, Nature Reviews Neuroscience.

[4]  G. Aston-Jones,et al.  Locus coeruleus neurons in monkey are selectively activated by attended cues in a vigilance task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  D. Paré,et al.  Amygdala Microcircuits Controlling Learned Fear , 2014, Neuron.

[6]  J. Cohen,et al.  The role of locus coeruleus in the regulation of cognitive performance. , 1999, Science.

[7]  J. D. McGaugh,et al.  Norepinephrine release in the amygdala in response to footshock and opioid peptidergic drugs , 1998, Brain Research.

[8]  G. Aghajanian,et al.  Evidence for norepinephrine-mediated collateral inhibition of locus coeruleus neurons , 1977, Brain Research.

[9]  Johannes J. Letzkus,et al.  Long-Range Connectivity Defines Behavioral Specificity of Amygdala Neurons , 2014, Neuron.

[10]  G. Aston-Jones,et al.  Afferent projections to the rat locus coeruleus demonstrated by retrograde and anterograde tracing with cholera-toxin B subunit and Phaseolus vulgaris leucoagglutinin , 1995, Neuroscience.

[11]  Yan Li,et al.  Norepinephrine enables the induction of associative long-term potentiation at thalamo-amygdala synapses , 2007, Proceedings of the National Academy of Sciences.

[12]  W. T. Nickell,et al.  The brain nucleus locus coeruleus: restricted afferent control of a broad efferent network. , 1986, Science.

[13]  Cyril Herry,et al.  Encoding of fear learning and memory in distributed neuronal circuits , 2014, Nature Neuroscience.

[14]  F. H. Do-Monte,et al.  Impairment of contextual conditioned fear extinction after microinjection of alpha-1-adrenergic blocker prazosin into the medial prefrontal cortex , 2010, Behavioural Brain Research.

[15]  S. Lammel,et al.  Reward and aversion in a heterogeneous midbrain dopamine system , 2014, Neuropharmacology.

[16]  Angela J. Yu,et al.  Uncertainty, Neuromodulation, and Attention , 2005, Neuron.

[17]  G. Aston-Jones,et al.  Conditioned responses of monkey locus coeruleus neurons anticipate acquisition of discriminative behavior in a vigilance task , 1997, Neuroscience.

[18]  S. Sara,et al.  Rapid habituation of auditory responses of locus coeruleus cells in anaesthetized and awake rats. , 1995, Neuroreport.

[19]  Carson C. Chow,et al.  Frequency-dependent synchrony in locus ceruleus: Role of electrotonic coupling , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[20]  H. Jelinek,et al.  Dye-coupling among neurons of the rat locus coeruleus during postnatal development , 1993, Neuroscience.

[21]  S. T. Mason,et al.  Learning in the absence of forebrain noradrenaline , 1975, Nature.

[22]  B. Waterhouse,et al.  Evidence for Broad Versus Segregated Projections from Cholinergic and Noradrenergic Nuclei to Functionally and Anatomically Discrete Subregions of Prefrontal Cortex , 2012, Front. Behav. Neurosci..

[23]  J. McGaughy,et al.  Atomoxetine reverses attentional deficits produced by noradrenergic deafferentation of medial prefrontal cortex , 2008, Psychopharmacology.

[24]  A. Grace,et al.  Noradrenergic Modulation of Basolateral Amygdala Neuronal Activity: Opposing Influences of α-2 and β Receptor Activation , 2007, The Journal of Neuroscience.

[25]  R C Lin,et al.  Lateralization and functional organization of the locus coeruleus projection to the trigeminal somatosensory pathway in rat , 1997, The Journal of comparative neurology.

[26]  E. V. Van Bockstaele,et al.  Endogenous opioids: The downside of opposing stress , 2014, Neurobiology of Stress.

[27]  Francisco Sotres-Bayon,et al.  Prefrontal control of fear: more than just extinction , 2010, Current Opinion in Neurobiology.

[28]  S. T. Mason,et al.  Locus coeruleus lesions: Learning and extinction , 1978, Physiology & Behavior.

[29]  C. Marsden,et al.  Effects of lesioning noradrenergic neurones in the locus coeruleus on conditioned and unconditioned aversive behaviour in the rat , 2001, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[30]  R. LaLumiere,et al.  The infralimbic cortex regulates the consolidation of extinction after cocaine self-administration. , 2010, Learning & memory.

[31]  J. D. McGaugh The amygdala modulates the consolidation of memories of emotionally arousing experiences. , 2004, Annual review of neuroscience.

[32]  G. Aston-Jones,et al.  Activation of monkey locus coeruleus neurons varies with difficulty and performance in a target detection task. , 2004, Journal of neurophysiology.

[33]  Jonathan D. Cohen,et al.  An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. , 2005, Annual review of neuroscience.

[34]  Joseph E LeDoux,et al.  Controlling the Elements: An Optogenetic Approach to Understanding the Neural Circuits of Fear , 2012, Biological Psychiatry.

[35]  J. Gold,et al.  Phasic Activation of Individual Neurons in the Locus Ceruleus/Subceruleus Complex of Monkeys Reflects Rewarded Decisions to Go But Not Stop , 2014, The Journal of Neuroscience.

[36]  E. V. Bockstaele,et al.  Light and electron microscopic evidence for topographic and monosynaptic projections from neurons in the ventral medulla to noradrenergic dendrites in the rat locus coeruleus , 1998, Brain Research.

[37]  B. Jacobs,et al.  Single unit activity of locus coeruleus neurons in the freely moving cat II. Conditioning and pharmacologic studies , 1986, Brain Research.

[38]  M. Segal,et al.  Plasticity of sensory responses of locus coeruleus neurons in the behaving rat: implications for cognition. , 1991, Progress in brain research.

[39]  Liqun Luo,et al.  Viral-genetic tracing of the input–output organization of a central norepinephrine circuit , 2015, Nature.

[40]  B. Berger,et al.  Biochemical and radioautographic evidence for dopaminergic afferents of the locus coeruleus originating in the ventral tegmental area , 2005, Journal of Neural Transmission.

[41]  Effects of lesions of the dorsal noradrenergic bundle on conditioned suppression to a CS and to a contextual background stimulus , 1989, Behavioural Brain Research.

[42]  S. Sara,et al.  Orienting and Reorienting: The Locus Coeruleus Mediates Cognition through Arousal , 2012, Neuron.

[43]  B. Waterhouse,et al.  Identification and distribution of projections from monoaminergic and cholinergic nuclei to functionally differentiated subregions of prefrontal cortex , 2013, Brain Research.

[44]  H. Eichenbaum,et al.  Noradrenergic, but not cholinergic, deafferentation of prefrontal cortex impairs attentional set-shifting , 2008, Neuroscience.

[45]  L. Thal,et al.  Comparison of the effects of single and combined neurotoxic lesions of the nucleus basalis magnocellularis and dorsal noradrenergic bundle on learning and memory in the rat , 1993, Behavioural Brain Research.

[46]  Joseph E LeDoux,et al.  Noradrenergic enhancement of reconsolidation in the amygdala impairs extinction of conditioned fear in rats—a possible mechanism for the persistence of traumatic memories in PTSD , 2011, Depression and anxiety.

[47]  S. Sara,et al.  Reward expectation, orientation of attention and locus coeruleus‐medial frontal cortex interplay during learning , 2004, The European journal of neuroscience.

[48]  J. Korf,et al.  Divergent axon collaterals of rat locus coeruleus neurons: demonstration by a fluorescent double labeling technique. , 1981, Brain research.

[49]  F. Chen,et al.  Locus coeruleus activation by foot shock or electrical stimulation inhibits amygdala neurons , 2007, Neuroscience.

[50]  E. V. Van Bockstaele,et al.  Hypothalamic projections to locus coeruleus neurons in rat brain , 2005, The European journal of neuroscience.

[51]  M. Ishimatsu,et al.  Synchronous Activity in Locus Coeruleus Results from Dendritic Interactions in Pericoerulear Regions , 1996, The Journal of Neuroscience.

[52]  K. Satoh,et al.  Divergent projections of catecholamine neurons of the locus coeruleus as revealed by fluorescent retrograde double labeling technique , 1981, Neuroscience Letters.

[53]  Kimberly L. Stachenfeld,et al.  Noradrenergic control of error perseveration in medial prefrontal cortex , 2013, Front. Integr. Neurosci..

[54]  Elyssa B. Margolis,et al.  Understanding opioid reward , 2015, Trends in Neurosciences.

[55]  J. Fallon,et al.  Catecholamine innervation of the basal forebrain III. Olfactory bulb, anterior olfactory nuclei, olfactory tubercle and piriform cortex , 1978, The Journal of comparative neurology.

[56]  B. Richmond,et al.  Sensitivity of Locus Ceruleus Neurons to Reward Value for Goal-Directed Actions , 2015, The Journal of Neuroscience.

[57]  B. Waterhouse,et al.  New perspectives on catecholaminergic regulation of executive circuits: evidence for independent modulation of prefrontal functions by midbrain dopaminergic and noradrenergic neurons , 2014, Front. Neural Circuits.

[58]  T. Robbins,et al.  Dissociable effects of lesions to the dorsal or ventral noradrenergic bundle on the acquisition, performance, and extinction of aversive conditioning. , 1987, Behavioral neuroscience.

[59]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[60]  D. Amaral,et al.  Locus coeruleus lesions and learning. , 1975, Science.

[61]  A. Arnsten Catecholamine Influences on Dorsolateral Prefrontal Cortical Networks , 2011, Biological Psychiatry.

[62]  Robert M Sears,et al.  Orexin/hypocretin system modulates amygdala-dependent threat learning through the locus coeruleus , 2013, Proceedings of the National Academy of Sciences.

[63]  D. Woodward,et al.  The distribution of neocortical projection neurons in the locus coeruleus , 1983, The Journal of comparative neurology.

[64]  S. T. Mason,et al.  Regional topography within noradrenergic locus coeruleus as revealed by retrograde transport of horseradish peroxidase , 1979, The Journal of comparative neurology.

[65]  F. Bloom,et al.  Nonrepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[66]  Joseph E LeDoux,et al.  Beta-Adrenergic Receptors in the Lateral Nucleus of the Amygdala Contribute to the Acquisition but Not the Consolidation of Auditory Fear Conditioning , 2010, Front. Behav. Neurosci..

[67]  B. Waterhouse,et al.  Topographic organization of rat locus coeruleus and dorsal raphe nuclei: Distribution of cells projecting to visual system structures , 1993, The Journal of comparative neurology.

[68]  B. Waterhouse,et al.  Heterogeneous organization of the locus coeruleus projections to prefrontal and motor cortices , 2014, Proceedings of the National Academy of Sciences.

[69]  T. Robbins,et al.  Enhanced behavioral conditioning to context and impaired behavioral and neuroendocrine responses to conditioned stimuli following ceruleocortical noradrenergic lesions: support for an attentional hypothesis of central noradrenergic function , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[70]  L. Swanson,et al.  The projections of the ventral tegmental area and adjacent regions: A combined fluorescent retrograde tracer and immunofluorescence study in the rat , 1982, Brain Research Bulletin.

[71]  G. Quirk,et al.  Noradrenergic Signaling in Infralimbic Cortex Increases Cell Excitability and Strengthens Memory for Fear Extinction , 2008, The Journal of Neuroscience.

[72]  S. Foote,et al.  Efferent projections of nucleus locus coeruleus: Morphologic subpopulations have different efferent targets , 1986, Neuroscience.

[73]  G. Aston-Jones,et al.  Evidence for self- and neighbor-mediated postactivation inhibition of locus coeruleus neurons , 1986, Brain Research.

[74]  J. Gray,et al.  Alleviation of response suppression to conditioned aversive stimuli by lesions of the dorsal noradrenergic bundle , 1984, Behavioural Brain Research.

[75]  R. North,et al.  Noradrenaline‐mediated synaptic inhibition in rat locus coeruleus neurones. , 1983, The Journal of physiology.

[76]  T. Sakurai,et al.  Orexin Receptor-1 in the Locus Coeruleus Plays an Important Role in Cue-Dependent Fear Memory Consolidation , 2013, The Journal of Neuroscience.

[77]  D. Jacobowitz,et al.  Serotonergic innervation of the forebrain: Effect of lesions on serotonin and tryptophan hydroxylase levels , 1977, Brain Research.

[78]  I. Izquierdo,et al.  Modulation of the extinction of two different fear-motivated tasks in three distinct brain areas , 2012, Behavioural Brain Research.

[79]  J. Fallon Collateralization of monoamine neurons: mesotelencephalic dopamine projections to caudate, septum, and frontal cortex , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[80]  K. Branson,et al.  Behavioral Variability through Stochastic Choice and Its Gating by Anterior Cingulate Cortex , 2014, Cell.

[81]  G. Aghajanian,et al.  Afferent projections to the rat locus coeruleus as determined by a retrograde tracing technique , 1978, The Journal of comparative neurology.

[82]  Andreas Lüthi,et al.  Neuronal circuits for fear and anxiety , 2015, Nature Reviews Neuroscience.

[83]  K. Svoboda,et al.  Genetic Dissection of Neural Circuits , 2008, Neuron.

[84]  J. Fallon,et al.  Catecholamine innervation of the basal forebrain II. Amygdala, suprarhinal cortex and entorhinal cortex , 1978, The Journal of comparative neurology.

[85]  J. D. McGaugh,et al.  Norepinephrine Release in the Amygdala in Response to Footshock Stimulation , 1996, Neurobiology of Learning and Memory.

[86]  E. V. Van Bockstaele,et al.  Amygdaloid Corticotropin‐Releasing Factor Targets Locus Coeruleus Dendrites: Substrate for the Co‐ordination of Emotional and Cognitive Limbs of the Stress Response , 1998, Journal of neuroendocrinology.

[87]  A. Arnsten Stress signalling pathways that impair prefrontal cortex structure and function , 2009, Nature Reviews Neuroscience.

[88]  P. Goldman-Rakic,et al.  Selective prefrontal cortical projections to the region of the locus coeruleus and raphe nuclei in the rhesus monkey , 1984, Brain Research.

[89]  Michael Davis,et al.  The amygdala: vigilance and emotion , 2001, Molecular Psychiatry.

[90]  S. T. Mason,et al.  THE EFFECTS OF DORSAL BUNDLE INJECTIONS OF 6‐HYDROXYDOPAMINE ON AVOIDANCE RESPONDING IN RATS , 1978, British journal of pharmacology.

[91]  M. Christie,et al.  Electrical coupling synchronizes subthreshold activity in locus coeruleus neurons in vitro from neonatal rats , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[92]  Joshua A. Gordon,et al.  Prefrontal entrainment of amygdala activity signals safety in learned fear and innate anxiety , 2013, Nature Neuroscience.

[93]  C. Berridge,et al.  The locus coeruleus–noradrenergic system: modulation of behavioral state and state-dependent cognitive processes , 2003, Brain Research Reviews.

[94]  James L. McGaugh,et al.  Enhancement of extinction memory consolidation: The role of the noradrenergic and GABAergic systems within the basolateral amygdala , 2006, Neurobiology of Learning and Memory.

[95]  S. Waddell Reinforcement signalling in Drosophila; dopamine does it all after all , 2013, Current Opinion in Neurobiology.

[96]  W. Kostowski,et al.  Locus coeruleus lesions and avoidance behavior in rats. , 1980, Acta neurobiologiae experimentalis.

[97]  K. Tye,et al.  From circuits to behaviour in the amygdala , 2015, Nature.

[98]  René Garcia,et al.  Time course of extracellular catecholamine and glutamate levels in the rat medial prefrontal cortex during and after extinction of conditioned fear , 2007, Synapse.

[99]  B. Jacobs,et al.  Single unit activity of locus coeruleus neurons in the freely moving cat I. During naturalistic behaviors and in response to simple and complex stimuli , 1986, Brain Research.

[100]  G. Harris,et al.  Locus coeruleus involvement in the learning of classically conditioned bradycardia , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[101]  Edward S Boyden,et al.  Hebbian and neuromodulatory mechanisms interact to trigger associative memory formation , 2014, Proceedings of the National Academy of Sciences.

[102]  J. Williams,et al.  Opioid inhibition in locus coeruleus. , 1995, Journal of neurophysiology.

[103]  G. Rubin,et al.  A subset of dopamine neurons signals reward for odour memory in Drosophila , 2012, Nature.

[104]  R. Joosten,et al.  Dopamine and noradrenaline efflux in the rat prefrontal cortex after classical aversive conditioning to an auditory cue , 2001, The European journal of neuroscience.

[105]  Joseph E LeDoux Emotion Circuits in the Brain , 2000 .

[106]  Shoji Nakamura,et al.  Antidromic activation of the rat locus coeruleus neurons from hippocampus, cerebral and cerebellar cortices , 1975, Brain Research.

[107]  Joseph E LeDoux,et al.  Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala , 2004, Neuroscience.

[108]  K. Deisseroth,et al.  Optogenetic investigation of neural circuits underlying brain disease in animal models , 2012, Nature Reviews Neuroscience.