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Dr Nathan Holmes

Dr Nathan Holmes

Lecturer

Research area and interest

I use animal models to study the behavioural and neurobiological substrates of attention, learning and memory. I am interested in the factors which regulate these processes in a normal brain, cause disturbances to these processes in a diseased brain, and the implications of these disturbances for disorders like post-traumatic stress (PTSD). In one line of inquiry, I study how basic information is processed in the brain, and how motivational states (like fear) change the way that information is processed. In a second line of inquiry, I study how the brain deals with contrasting information, and the role of context in processing this information.
Email

n.holmes@unsw.edu.au

Location

Mathews, Room 909

Publications

Journal articles

  • 1.ÌýÌýÌýÌýÌýÌýÌýÌýCrane, J. W.,ÌýHolmes,ÌýN. M., Fam, J.,ÌýWestbrook,ÌýR. F., & Delaney, A. J. (2020).ÌýÌýJournal of Neurophysiology,Ìý123(2):587-599. doi: 10.1152/jn.00571.2019.
  • 2.ÌýÌýÌýÌýÌýÌýÌýÌýWilliams-Spooner, M. J., Westbrook, R. F., &ÌýHolmes, N. M.Ìý(2019). The conditions under which consolidation of serial-order conditioned fear requiresÌýde novoÌýprotein synthesis in the basolateral amygdala complex.ÌýJournal of Neuroscience,Ìý39(37): 7357-7368. doi: 10.1523/JNEUROSCI.0768-19.2019. Epub 2019 Jul 24.
  • 3.ÌýÌýÌýÌýÌýÌýÌýÌýWong, F. S., Westbrook, R. F., &ÌýHolmes, N. M.Ìý(2019). ‘Online’ integration of sensory and fear memories in the rat medial temporal lobe.ÌýeLife, Jun 10;8. pii: e47085. doi: 10.7554/eLife.47085.
  • 4.ÌýÌýÌýÌýÌýÌýÌýÌýHolmes, N. M., Chan, Y. Y., & Westbrook, R. F. (2019). A combination of common and individual error terms is not needed to explain associative changes when cues with different training histories are conditioned in compound: A review of Rescorla’s compound test procedure.ÌýJournal of Experimental Psychology: Animal Learning & Cognition,Ìý45(2), 242-56.
  • 5.ÌýÌýÌýÌýÌýÌýÌýÌýHolmes, N. M., Pan, J., Davis, A., Panayi, M. C., & Clemens, K. J. (2018). Rats choose high doses of nicotine in order to compensate for changes in its price and availability.ÌýAddiction Biology,Ìý24, 849-859.
  • 6.ÌýÌýÌýÌýÌýÌýÌýÌýLingawi, N. W., Andrew, E., Laurent, V., Killcross, A. S., Westbrook, R. F., &ÌýHolmes, N. M.Ìý(2018). The conditions that regulate formation of a false fear memory in rats.ÌýNeurobiology of Learning and Memory, 156,Ìý53-59.
  • 7.ÌýÌýÌýÌýÌýÌýÌýÌýLingawi, N. W., Laurent, V., Westbrook, R. F., &ÌýHolmes, N. M.Ìý(2018). The role of the basolateral amygdala and infralimbic cortex in (re)learning extinction.ÌýPsychopharmacology,Ìý236, 303-312.
  • 8.ÌýÌýÌýÌýÌýÌýÌýÌýLeidl, D. M., Lay, B. P. P., Chakouch, C., Westbrook, R. F., &ÌýHolmes,Ìý N. M.Ìý(2018). Protein synthesis in the basolateral amygdala complex is required for consolidation of a first-order fear memory, but not for consolidation of a higher-order fear memory.ÌýNeurobiology of Learning and Memory,Ìý153, 153-165.
  • 9.ÌýÌýÌýÌýÌýÌýÌýÌýFam, J.,ÌýHolmes, N. M., Crane, J. W, Delaney, A. J., & Westbrook, R. F. (2018).ÌýOxytocin receptor activation in the basolateral complex of the amygdala enhances discrimination between discrete cues and promotes configural processing of cues.ÌýPsychoneuroendocrinology, 96, 84-92.
  • 10.ÌýÌýÌýÌýÌýDelaney, A. J., Crane, J. W., Fam, J.,ÌýHolmes, N. M., & Westbrook, R. F. (2018). Baclofen acts in the central amygdala to reduce synaptic transmission and impair context fear conditioning.ÌýScientific Reports,Ìý2018 Jul 2;8(1):9908. doi: 10.1038/s41598-018-28321-0.
  • 11.ÌýÌýÌýÌýÌýLingawi, N. W.,ÌýHolmes, N. M.,ÌýWestbrook, R. F., & Laurent, V. (2018). The infralimbic cortex encodes inhibition irrespective of motivational significance.ÌýNeurobiology of Learning and Memory, 150, 64-74.
  • 12.ÌýÌýÌýÌýÌýLay, B. P. P., Westbrook, R. F., Glanzman, D. L., &ÌýHolmes, N. M.Ìý(2018). Commonalities and differences in the substrates underlying consolidation of first- and second-order conditioned fear.ÌýJournal of Neuroscience, 38,Ìý1926-1941. doi: 10.1523/JNEUROSCI.2966-17.2018.
  • 13.ÌýÌýÌýÌýÌýHolmes, N. M., Raipuria, M., Qureshi, O., Killcross, A. S., & Westbrook, R. F. (2018). Danger changes the way the mammalian brain stores information about innocuous events: a study of sensory preconditioning in rats.ÌýeNeuro, 0381-17.2017.
  • 14.ÌýÌýÌýÌýÌýClemens, K. J., &ÌýHolmes, N. M.Ìý(2017). An extended history of drug self-administration results in multiple sources of control over drug seeking behaviour.ÌýProgress in Neuropsychopharmacology and Biological Psychiatry, Nov 10. pii: S0278-5846(17)30418-9. doi: 10.1016/j.pnpbp.2017.11.011. [Epub ahead of print].
  • 15.ÌýÌýÌýÌýÌýHolmes, N. M.,ÌýCrane, J. W., Tang, M., Fam, J., Westbrook, R. F., & Delaney, A. J. (2017). α2-adrenoceptor-mediated inhibition in the central amygdala blocks fear-conditioning.ÌýScientific Reports,Ìý2017 Sep 15;7(1):11712. doi: 10.1038/s41598-017-12115-x.
  • 16.ÌýÌýÌýÌýÌýHolmes, N. M.,Ìý& Westbrook, R. F. (2017). A dangerous context changes the way that rats learn about and discriminate between innocuous events in sensory preconditioning.ÌýLearning and Memory, 24(9), 440-448.
  • 17.ÌýÌýÌýÌýÌýFam, J., Westbrook, R. F., &ÌýHolmes, N. M.Ìý(2017). An examination of changes in behavioural control when stimuli with different associative histories are conditioned in compound.ÌýJournal of Experimental Psychology: Animal Learning & Cognition,Ìý43(3), 205-18.
  • 18.ÌýÌýÌýÌýÌýGriffiths, O,ÌýHolmes, N. M.,Ìý& Westbrook, R. F. (2017). Compound stimulus presentation does not deepen extinction in human causal learning.ÌýFrontiers in Psychology,ÌýFeb 9;8:120. doi: 10.3389/fpsyg.2017.00120. eCollection 2017
  • 19.ÌýÌýÌýÌýÌýHolmes, N. M.,ÌýHutton-Bedbrook, K., Fam, J., & Westbrook, R. F. (2016). Incentive contrast effects regulate responding to a flavor presented in compound with a saccharin unconditioned stimulus in rats.ÌýJournal of Experimental Psychology: Animal Learning & Cognition,Ìý42(3), 233-45.
  • 20.ÌýÌýÌýÌýÌýHolmes, N. M.,ÌýLeung, H. T., & Westbrook, R. F. (2016). Counter-conditioned fear responses exhibit greater renewal than extinguished fear responses.ÌýLearning & Memory, 23(4), 141-50.
  • 21.ÌýÌýÌýÌýÌýLeung, H. T.,ÌýHolmes, N. M.,Ìý& Westbrook. R. F. (2016). An appetitive conditioned stimulus enhances acquisition and impairs extinction of conditioned fear in rats.ÌýLearning & Memory, 23(3), 113-20.
  • 22.ÌýÌýÌýÌýÌýMacnamara, C. L.,ÌýHolmes, N. M.,ÌýWestbrook, R. F., & Clemens, K. J. (2016). Varenicline impairs extinction and enhances reinstatement across repeated cycles of nicotine self-administration in rats.ÌýNeuropharmacology,Ìý105, 463-70.
  • 23.ÌýÌýÌýÌýÌýClemens, K. J., Lay, B.Ìý P. P., &ÌýHolmes, N. M.Ìý(2015). Extended nicotine self-administration increases sensitivity to nicotine, motivation to seek nicotine, and the reinforcing properties of nicotine-paired cues.ÌýAddiction Biology.Ìý(in press).
  • 24.ÌýÌýÌýÌýÌýBae, S. E.,ÌýHolmes, N. M.,Ìý& Westbrook. R. F. (2015). False context fear memory in rats.ÌýLearning & Memory,Ìý22(10), 519-525.
  • 25.ÌýÌýÌýÌýÌýCampbell-Smith, E. J.,ÌýHolmes, N. M., Lingawi, N. W., Panayi, M. C., & Westbrook, R. F. (2015). Oxytocin signalling in basolateral and central amygdala nuclei differentially regulates the acquisition, expression and extinction of context conditioned fear in rats.ÌýLearning & Memory,Ìý22(5), 245-57.
  • 26.ÌýÌýÌýÌýÌýHart, G.,ÌýHolmes, N. M., Harris, J. A., & Westbrook, R. F. (2014). Benzodiazepine administration prevents the use of error-correction mechanisms during fear extinction.ÌýLearning & Behavior,Ìý42(4), 383-97.
  • 27.ÌýÌýÌýÌýÌýHolmes, N. M., & Westbrook, R. F. (2014). Appetitive context conditioning proactively, but transiently, interferes with expression of counter-conditioned context fear.ÌýLearning & Memory,Ìý21(11), 597-605.
  • 28.ÌýÌýÌýÌýÌýHolmes, N. M.,ÌýCai, S. Y., Lay, B. P. P., Watts, N. R., & Westbrook, R. F. (2014). Extinguished second-order fear responses are renewed but not reinstated.ÌýJournal of Experimental Psychology: Animal Learning & Cognition,Ìý40(4), 440-458.
  • 29.ÌýÌýÌýÌýÌýHolmes, N. M.,ÌýGriffiths, O., & Westbrook, R. F. (2014). The influence of partner cues on extinction of causal judgments in people.ÌýLearning & Behavior,Ìý42(3), 289-303.
  • 30.ÌýÌýÌýÌýÌýClemens, K. J., Castino, M. R., Cornish, J. L., Goodchild, A. K., &ÌýHolmes, N. M.Ìý(2014). Behavioral and neural substrates of habit formation in rats intravenously self-administering nicotine.ÌýNeuropsychopharmacology, 39(11), 2584-93.
  • 31.ÌýÌýÌýÌýÌýHolmes, N. M.,ÌýSouth, T., Martire, S. I., Westbrook, R. F., & Morris, M. J. (2014). Rats eat a cafeteria-style diet to excess, but eat smaller amounts and less frequently when tested with chow. PLoS ONE, 9(4), e93506.
  • 32.ÌýÌýÌýÌýÌýHolmes, N. M.,Ìý& Westbrook, R. F. (2014). ABA renewal is greater when extinction occurs in the same context as cue pre-exposure.ÌýJournal of Experimental Psychology: Animal Learning & Cognition,Ìý40(3), 369-79.
  • 33.ÌýÌýÌýÌýÌýMartire, S. I., Maniam, J., South, T.,ÌýHolmes, N. M.,ÌýWestbrook, R. F., & Morris, M. J. (2014). Extended exposure to a palatable cafeteria diet alters gene expression in brain regions implicated in reward, and withdrawal from this diet alters gene expression in brain regions associated with stress.ÌýBehavioural Brain Research,Ìý265, 132-41.
  • 34.ÌýÌýÌýÌýÌýHolmes, N. M.,ÌýParkes, S. L., Killcross, A. S., & Westbrook, R. F. (2013). The basolateral amygdala is critical for learning about neutral stimuli in the presence of danger, and the perirhinal cortex is critical in the absence of danger.ÌýJournal of Neuroscience,Ìý33(32), 13112-25.
  • 35.ÌýÌýÌýÌýÌýHolmes, N. M.,Ìý& Fam, J. (2013). How does dopamine release in the nucleus accumbens core relate to encoding of a Pavlovian incentive stimulus?ÌýJournal of Neuroscience,Ìý33(25), 10191-2.
  • 36.ÌýÌýÌýÌýÌýHolmes, N. M.,Ìý& Westbrook, R. F. (2013) Extinction of reinstated or ABC renewed fear responses renders them resistant to subsequent ABA renewal.ÌýJournal of Experimental Psychology: Animal Behavior Processes, 39(3), 208-220.
  • 37.ÌýÌýÌýÌýÌýMartire, S. I.,ÌýHolmes, N. M., Westbrook, R. F., & Morris, M. J. (2013). Altered feeding patterns in rats exposed to a cafeteria diet: increased snacking and its implications for development of obesity. PLoS ONE, DOI: 10.1371/journal.pone.0060407.
  • 38.ÌýÌýÌýÌýÌýRosenberg, H.,ÌýHolmes, N. M., Harris, J. A., & Westbrook, R. F. (2011). Pre-exposure enhances recovery of conditioned responding after extinction.ÌýLearning & Behavior,Ìý39(3), 212-23.
  • 39.ÌýÌýÌýÌýÌýHolmes, N. M., & Clemens, K. J. (2011). Multiple interpretations of cocaine-seeking behaviour after prolonged self-administration training.ÌýJournal of Neuroscience,Ìý31(11), 3935-6.
  • 40.ÌýÌýÌýÌýÌýHolmes, N. M., Marchand, A. R., & Coutureau, E. (2010). Pavlovian to instrumental transfer: A neurobehavioural perspective.ÌýNeuroscience & Biobehavioral Reviews, 34(8), 1277-95.
  • 41.ÌýÌýÌýÌýÌýHoltzman, O., Siette, J.,ÌýHolmes, N. M., & Westbrook, R. F. (2010). Additional exposures reverse the latent inhibitory effects of recent and remote exposures.ÌýJournal of Experimental Psychology: Animal Behavior Processes, 36(3), 368-80.
  • 42.ÌýÌýÌýÌýHolmes, N. M., & Harris, J. A. (2009). The loss of latent inhibition across compound conditioning.ÌýJournal of Experimental Psychology: Animal Behavior Processes, 35(3), 328-39.

Book Chapters

  • Holmes, N. M.Ìý&Harris, J. A. (2010). Latent inhibition. InÌýAttention and Associative Learning: From Brain to Behaviour, Le Pelley, M., & Mitchell, C. (Eds.). Oxford University Press.

Awards, fellowships & grants

2020 – 2023ÌýÌýAustralian Research Council Future Fellowship.ÌýThe processing of fear in the medial temporal lobe. ($798,704).ÌýPrincipal Investigator

2020 – 2022ÌýÌýAustralian Research Council Discovery Project.ÌýExtinction of fears based on learned sources of danger. ($370,000).ÌýLead Investigator

2019 – 2021ÌýÌýAustralian Research Council Discovery Project.ÌýHow an innocuous event never associated with danger becomes frightening. ($335,000).ÌýLead Investigator

2018 – 2020ÌýÌýNational Health and Medical Research Council Project Grant.ÌýModelling post-traumatic stress in rats: hypervigilance and the spread of fear. ($348,000).ÌýChief Investigator (CIA)

2016 – 2018ÌýÌýAustralian Research Council Discovery Project.ÌýThe neural substrates of false fear memory in rats. ($426,000).ÌýLead Investigator

2015 – 2017ÌýÌýAustralian Research Council Discovery Early Career Research AwardÌý(DECRA). Fear changes how the brain processes innocuous information. ($375,000).ÌýPrincipal Investigator

2015 – 2017ÌýÌýNational Health and Medical Research Council Project Grant.ÌýOxytocin impairs fear acquisition and enhances fear inhibition: mechanisms of action in the basolateral complex of the amygdala. ($390,000).ÌýChief Investigator (CIB)

Affiliations & memberships

Society for Neuroscience (SfN)

Australian Neuroscience Society (ANS)

Australian Learning Group (ALG)

French Neuroscience Society (past)

Current PhD Students

1.ÌýÌýÌýÌýÌýÌýÌýDana LeidlÌý(Start in 2018). First and second-order fear memories are encoded in overlapping populations of neurons in the basolateral amygdala complex.Ìý91É«ÇéƬ Scientia PhD Scholar.

2.ÌýÌýÌýÌýÌýÌýÌýÌýArtur ShvetcovÌý(Start in 2018). The molecular substrates of second-order conditioned fear in the basolateral amygdala complex.

3.ÌýÌýÌýÌýÌýÌýÌýÌýFrancesca WongÌý(Start in 2018). The role of the perirhinal cortex in the integration of distinct sources of information in a sensory preconditioning procedure.

4.ÌýÌýÌýÌýÌýÌýÌýYvonne Chan(Start in 2018). The roles of the basolateral amygdala complex and infralimbic cortex in extinction and re-extinction of conditioned fear.

5.ÌýÌýÌýÌýÌýÌýÌýÌýOmar QureshiÌý(Start in 2017). The effect of gradually reducing an established CS-US contingency on the subsequent extinction of conditioned responding.

6.ÌýÌýÌýÌýÌýÌýÌýÌýMathew Williams-SpoonerÌý(Start in 2017). The conditions under which protein synthesis is required for consolidation of fear memories in the basolateral amygdala complex.

Past PhD Students

Belinda Po Pyn LayÌý(2012-16). The role of the basolateral amygdala complex in consolidation of second-order conditioned fear.ÌýJointly supervised with Prof Fred Westbrook.

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