Get access

Primary and secondary neural networks of auditory prepulse inhibition: a functional magnetic resonance imaging study of sensorimotor gating of the human acoustic startle response

Authors

  • Linda E. Campbell,

    1. Schizophrenia Research Institute, Sydney, Australia
    2. Centre for Brain & Mental Health Research, The University of Newcastle and Hunter Medical Research Institute, Newcastle, Australia
    Search for more papers by this author
  • Matthew Hughes,

    1. Schizophrenia Research Institute, Sydney, Australia
    2. Centre for Brain & Mental Health Research, The University of Newcastle and Hunter Medical Research Institute, Newcastle, Australia
    Search for more papers by this author
  • Timothy W. Budd,

    1. Schizophrenia Research Institute, Sydney, Australia
    2. Centre for Brain & Mental Health Research, The University of Newcastle and Hunter Medical Research Institute, Newcastle, Australia
    Search for more papers by this author
  • Gavin Cooper,

    1. Schizophrenia Research Institute, Sydney, Australia
    2. Centre for Brain & Mental Health Research, The University of Newcastle and Hunter Medical Research Institute, Newcastle, Australia
    Search for more papers by this author
  • W. Ross Fulham,

    1. Schizophrenia Research Institute, Sydney, Australia
    2. Centre for Brain & Mental Health Research, The University of Newcastle and Hunter Medical Research Institute, Newcastle, Australia
    Search for more papers by this author
  • Frini Karayanidis,

    1. Schizophrenia Research Institute, Sydney, Australia
    2. Centre for Brain & Mental Health Research, The University of Newcastle and Hunter Medical Research Institute, Newcastle, Australia
    Search for more papers by this author
  • Mary-Claire Hanlon,

    1. Schizophrenia Research Institute, Sydney, Australia
    2. Centre for Brain & Mental Health Research, The University of Newcastle and Hunter Medical Research Institute, Newcastle, Australia
    Search for more papers by this author
  • Wendy Stojanov,

    1. Centre for Brain & Mental Health Research, The University of Newcastle and Hunter Medical Research Institute, Newcastle, Australia
    Search for more papers by this author
  • Patrick Johnston,

    1. Brain Sciences Institute, Swinburne University of Technology, Melbourne, Australia
    Search for more papers by this author
  • Vanessa Case,

    1. Schizophrenia Research Institute, Sydney, Australia
    2. Centre for Brain & Mental Health Research, The University of Newcastle and Hunter Medical Research Institute, Newcastle, Australia
    Search for more papers by this author
  • Ulrich Schall

    1. Schizophrenia Research Institute, Sydney, Australia
    2. Centre for Brain & Mental Health Research, The University of Newcastle and Hunter Medical Research Institute, Newcastle, Australia
    Search for more papers by this author

Dr U. Schall, as above.
E-mail: Ulrich.Schall@newcastle.edu.au

Abstract

Feedforward inhibition deficits have been consistently demonstrated in a range of neuropsychiatric conditions using prepulse inhibition (PPI) of the acoustic startle eye-blink reflex when assessing sensorimotor gating. While PPI can be recorded in acutely decerebrated rats, behavioural, pharmacological and psychophysiological studies suggest the involvement of a complex neural network extending from brainstem nuclei to higher order cortical areas. The current functional magnetic resonance imaging study investigated the neural network underlying PPI and its association with electromyographically (EMG) recorded PPI of the acoustic startle eye-blink reflex in 16 healthy volunteers. A sparse imaging design was employed to model signal changes in blood oxygenation level-dependent (BOLD) responses to acoustic startle probes that were preceded by a prepulse at 120 ms or 480 ms stimulus onset asynchrony or without prepulse. Sensorimotor gating was EMG confirmed for the 120-ms prepulse condition, while startle responses in the 480-ms prepulse condition did not differ from startle alone. Multiple regression analysis of BOLD contrasts identified activation in pons, thalamus, caudate nuclei, left angular gyrus and bilaterally in anterior cingulate, associated with EMG-recorded sensorimotor gating. Planned contrasts confirmed increased pons activation for startle alone vs 120-ms prepulse condition, while increased anterior superior frontal gyrus activation was confirmed for the reverse contrast. Our findings are consistent with a primary pontine circuitry of sensorimotor gating that interconnects with inferior parietal, superior temporal, frontal and prefrontal cortices via thalamus and striatum. PPI processes in the prefrontal, frontal and superior temporal cortex were functionally distinct from sensorimotor gating.

Ancillary