Dr Nathan Holmes

Dr Nathan Holmes


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.


Mathews, Room 909


Journal articles

  • 1.        Crane, J. W., Holmes, N. M., Fam, J., Westbrook, R. F., & Delaney, A. J. (2020). Oxytocin increases inhibitory synaptic transmission and blocks development of long-term potentiation in the lateral amygdala. Journal of Neurophysiology, 123(2):587-599. doi: 10.1152/jn.00571.2019.
  • 2.        Williams-Spooner, M. J., Westbrook, R. F., & Holmes, N. M. (2019). The conditions under which consolidation of serial-order conditioned fear requires de novo protein synthesis in the basolateral amygdala complex. Journal of Neuroscience39(37): 7357-7368. doi: 10.1523/JNEUROSCI.0768-19.2019. Epub 2019 Jul 24.
  • 3.        Wong, F. S., Westbrook, R. F., & Holmes, N. M. (2019). ‘Online’ integration of sensory and fear memories in the rat medial temporal lobe. eLife, Jun 10;8. pii: e47085. doi: 10.7554/eLife.47085.
  • 4.        Holmes, 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. Journal of Experimental Psychology: Animal Learning & Cognition, 45(2), 242-56.
  • 5.        Holmes, 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. Addiction Biology24, 849-859.
  • 6.        Lingawi, N. W., Andrew, E., Laurent, V., Killcross, A. S., Westbrook, R. F., & Holmes, N. M. (2018). The conditions that regulate formation of a false fear memory in rats. Neurobiology of Learning and Memory, 156, 53-59.
  • 7.        Lingawi, N. W., Laurent, V., Westbrook, R. F., & Holmes, N. M. (2018). The role of the basolateral amygdala and infralimbic cortex in (re)learning extinction. Psychopharmacology, 236, 303-312.
  • 8.        Leidl, D. M., Lay, B. P. P., Chakouch, C., Westbrook, R. F., & Holmes,  N. M. (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. Neurobiology of Learning and Memory153, 153-165.
  • 9.        Fam, J., Holmes, N. M., Crane, J. W, Delaney, A. J., & Westbrook, R. F. (2018). Oxytocin receptor activation in the basolateral complex of the amygdala enhances discrimination between discrete cues and promotes configural processing of cues. Psychoneuroendocrinology, 96, 84-92.
  • 10.     Delaney, A. J., Crane, J. W., Fam, J., Holmes, N. M., & Westbrook, R. F. (2018). Baclofen acts in the central amygdala to reduce synaptic transmission and impair context fear conditioning. Scientific Reports, 2018 Jul 2;8(1):9908. doi: 10.1038/s41598-018-28321-0.
  • 11.     Lingawi, N. W., Holmes, N. M., Westbrook, R. F., & Laurent, V. (2018). The infralimbic cortex encodes inhibition irrespective of motivational significance. Neurobiology of Learning and Memory, 150, 64-74.
  • 12.     Lay, B. P. P., Westbrook, R. F., Glanzman, D. L., & Holmes, N. M. (2018). Commonalities and differences in the substrates underlying consolidation of first- and second-order conditioned fear. Journal of Neuroscience, 38, 1926-1941. doi: 10.1523/JNEUROSCI.2966-17.2018.
  • 13.     Holmes, 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. eNeuro, 0381-17.2017.
  • 14.     Clemens, K. J., & Holmes, N. M. (2017). An extended history of drug self-administration results in multiple sources of control over drug seeking behaviour. Progress 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.     Holmes, N. M., Crane, J. W., Tang, M., Fam, J., Westbrook, R. F., & Delaney, A. J. (2017). α2-adrenoceptor-mediated inhibition in the central amygdala blocks fear-conditioning. Scientific Reports, 2017 Sep 15;7(1):11712. doi: 10.1038/s41598-017-12115-x.
  • 16.     Holmes, N. M., & Westbrook, R. F. (2017). A dangerous context changes the way that rats learn about and discriminate between innocuous events in sensory preconditioning. Learning and Memory, 24(9), 440-448.
  • 17.     Fam, J., Westbrook, R. F., & Holmes, N. M. (2017). An examination of changes in behavioural control when stimuli with different associative histories are conditioned in compound. Journal of Experimental Psychology: Animal Learning & Cognition, 43(3), 205-18.
  • 18.     Griffiths, O, Holmes, N. M., & Westbrook, R. F. (2017). Compound stimulus presentation does not deepen extinction in human causal learning. Frontiers in Psychology, Feb 9;8:120. doi: 10.3389/fpsyg.2017.00120. eCollection 2017
  • 19.     Holmes, N. M., Hutton-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. Journal of Experimental Psychology: Animal Learning & Cognition, 42(3), 233-45.
  • 20.     Holmes, N. M., Leung, H. T., & Westbrook, R. F. (2016). Counter-conditioned fear responses exhibit greater renewal than extinguished fear responses. Learning & Memory, 23(4), 141-50.
  • 21.     Leung, H. T., Holmes, N. M., & Westbrook. R. F. (2016). An appetitive conditioned stimulus enhances acquisition and impairs extinction of conditioned fear in rats. Learning & Memory, 23(3), 113-20.
  • 22.     Macnamara, C. L., Holmes, N. M., Westbrook, R. F., & Clemens, K. J. (2016). Varenicline impairs extinction and enhances reinstatement across repeated cycles of nicotine self-administration in rats. Neuropharmacology, 105, 463-70.
  • 23.     Clemens, K. J., Lay, B.  P. P., & Holmes, N. M. (2015). Extended nicotine self-administration increases sensitivity to nicotine, motivation to seek nicotine, and the reinforcing properties of nicotine-paired cues. Addiction Biology. (in press).
  • 24.     Bae, S. E., Holmes, N. M., & Westbrook. R. F. (2015). False context fear memory in rats. Learning & Memory, 22(10), 519-525.
  • 25.     Campbell-Smith, E. J., Holmes, 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. Learning & Memory, 22(5), 245-57.
  • 26.     Hart, G., Holmes, N. M., Harris, J. A., & Westbrook, R. F. (2014). Benzodiazepine administration prevents the use of error-correction mechanisms during fear extinction. Learning & Behavior, 42(4), 383-97.
  • 27.     Holmes, N. M., & Westbrook, R. F. (2014). Appetitive context conditioning proactively, but transiently, interferes with expression of counter-conditioned context fear. Learning & Memory, 21(11), 597-605.
  • 28.     Holmes, N. M., Cai, S. Y., Lay, B. P. P., Watts, N. R., & Westbrook, R. F. (2014). Extinguished second-order fear responses are renewed but not reinstated. Journal of Experimental Psychology: Animal Learning & Cognition, 40(4), 440-458.
  • 29.     Holmes, N. M., Griffiths, O., & Westbrook, R. F. (2014). The influence of partner cues on extinction of causal judgments in people. Learning & Behavior, 42(3), 289-303.
  • 30.     Clemens, K. J., Castino, M. R., Cornish, J. L., Goodchild, A. K., & Holmes, N. M. (2014). Behavioral and neural substrates of habit formation in rats intravenously self-administering nicotine. Neuropsychopharmacology, 39(11), 2584-93.
  • 31.     Holmes, N. M., South, 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.     Holmes, N. M., & Westbrook, R. F. (2014). ABA renewal is greater when extinction occurs in the same context as cue pre-exposure. Journal of Experimental Psychology: Animal Learning & Cognition, 40(3), 369-79.
  • 33.     Martire, S. I., Maniam, J., South, T., Holmes, N. M., Westbrook, 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. Behavioural Brain Research, 265, 132-41.
  • 34.     Holmes, N. M., Parkes, 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. Journal of Neuroscience, 33(32), 13112-25.
  • 35.     Holmes, N. M., & Fam, J. (2013). How does dopamine release in the nucleus accumbens core relate to encoding of a Pavlovian incentive stimulus? Journal of Neuroscience, 33(25), 10191-2.
  • 36.     Holmes, N. M., & Westbrook, R. F. (2013) Extinction of reinstated or ABC renewed fear responses renders them resistant to subsequent ABA renewal. Journal of Experimental Psychology: Animal Behavior Processes, 39(3), 208-220.
  • 37.     Martire, S. I., Holmes, 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.     Rosenberg, H., Holmes, N. M., Harris, J. A., & Westbrook, R. F. (2011). Pre-exposure enhances recovery of conditioned responding after extinction. Learning & Behavior, 39(3), 212-23.
  • 39.     Holmes, N. M., & Clemens, K. J. (2011). Multiple interpretations of cocaine-seeking behaviour after prolonged self-administration training. Journal of Neuroscience, 31(11), 3935-6.
  • 40.     Holmes, N. M., Marchand, A. R., & Coutureau, E. (2010). Pavlovian to instrumental transfer: A neurobehavioural perspective. Neuroscience & Biobehavioral Reviews, 34(8), 1277-95.
  • 41.     Holtzman, O., Siette, J., Holmes, N. M., & Westbrook, R. F. (2010). Additional exposures reverse the latent inhibitory effects of recent and remote exposures. Journal of Experimental Psychology: Animal Behavior Processes, 36(3), 368-80.
  • 42.    Holmes, N. M., & Harris, J. A. (2009). The loss of latent inhibition across compound conditioning. Journal of Experimental Psychology: Animal Behavior Processes, 35(3), 328-39.

Book Chapters

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

Awards, fellowships & grants

2020 – 2023  Australian Research Council Future Fellowship. The processing of fear in the medial temporal lobe. ($798,704). Principal Investigator

2020 – 2022  Australian Research Council Discovery Project. Extinction of fears based on learned sources of danger. ($370,000). Lead Investigator

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

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

2016 – 2018  Australian Research Council Discovery Project. The neural substrates of false fear memory in rats. ($426,000). Lead Investigator

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

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

Affiliations & memberships

Society for Neuroscience (SfN)

Australian Neuroscience Society (ANS)

Australian Learning Group (ALG)

French Neuroscience Society (past)

Current PhD Students

1.       Dana Leidl (Start in 2018). First and second-order fear memories are encoded in overlapping populations of neurons in the basolateral amygdala complex. UNSW Scientia PhD Scholar.

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

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

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

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

6.        Mathew Williams-Spooner (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 Lay (2012-16). The role of the basolateral amygdala complex in consolidation of second-order conditioned fear. Jointly supervised with Prof Fred Westbrook.