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The role of sensory pathways in Pavlovian conditioning in rabbit

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Abstract

In an earlier experiment we showed that selective attention plays a critical role in rabbit eye blink conditioning (Steele-Russell et al. in Exp Brain Res 173:587–602, 2006). The present experiments are concerned to examine the extent to which visual recognition processes are a separate component from the motor learning that is also involved in conditioning. This was achieved by midline section of the optic chiasma which disconnected the direct retinal projections via the brainstem to the cerebellar oculomotor control system. By comparing both normal and chiasma-sectioned rabbits it was possible to determine the dependence or independence of conditioning on the motor expression of the eye blink response during training. Both normal and chiasma-sectioned animals were tested using a multiple test battery to determine the effect of this redirection of the visual input pathways on conditioning. All animals were first tested for any impairment in visual capability following section of the optic chiasma. Despite the loss of 90% of retinal ganglion cell fibres, no visual impairment for either intensity or pattern vision was seen in the chiasma animals. Also no difference was seen in nictitating membrane (NM) conditioning to an auditory signal between normal and chiasma animals. Testing for motor learning to a visual signal, the chiasma rabbits showed a complete lack of any NM conditioning. However the sensory tests of visual conditioning showed that chiasma-sectioned animals had completely normal sensory recognition learning. These results show that NM Pavlovian conditioning involves anatomically separate and independent sensory recognition and motor output components of the learning.

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Abbreviations

ANOVA:

Analysis of variance

CR:

Conditional response

CS:

Conditional stimulus

DPFl:

Dorsal paraflocculus

HVI:

Cerebellar vermal lobus simplex

HVII:

Vermal lobule

ITI:

Intertrial interval

LDN:

Lateral dorsal nucleus of the accessory optic system

LGN:

Lateral geniculate nucleus of the thalamus

LTN:

Lateral terminal nucleus of the accessory optic system

P cells:

Retinal ganglion cells which in monkey and human project to the parvo- cellular layers of the LGN

M cell:

Retinal ganglion cells which in monkey and human project to the magno-cellular layers of the LGN

MST:

Region in parietal cortex anterior to MT

MT:

Region in parietal extrastriate cortex

MTN:

Medial terminal nucleus of the accessory optic system

NOT:

Nucleus of the optic tract

NP:

Pontine nucleus

SPL:

Sound pressure level

S+ :

Correct stimulus

S− :

Incorrect stimulus

SPEM:

Smooth pursuit eye movements

UR:

Unconditional response

X cells:

Retinal ganglion cells with small receptive fields tuned to patterns

Y cells:

Retinal ganglion cells with large receptive fields tuned to motion

V1 :

Brodman area 17 of the visual cortex

V2 :

Brodman area 18 of the visual cortex

VOR:

Vestibulo ocular reflex

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Acknowledgments

The authors would like to express their gratitude to Anthony Dickenson (University of Cambridge), Robert Doty (University of Rochester), Bryan Smotherman (Texas A&M University), Christopher Yeo (University College London), for their careful reading of earlier versions of the manuscript as well as for their thoughtful advice and criticism.

Author information

Authors and Affiliations

  1. Sensory Neuroscience Laboratory, Texas A&M University, College Station, TX, 77843, USA

    I. Steele-Russell, M. I. Russell & J. A. Castiglioni

  2. Department of Psychiatry and Behavioral Science, Texas A&M University, College Station, TX, 77843, USA

    I. Steele-Russell & J. A. Castiglioni

  3. Department of Neuroscience & Experimental Therapeutics, Texas A&M University, College Station, TX, 77843, USA

    I. Steele-Russell

  4. Department Veterinary Integrative Biosciences, TAMUS HSC and S&W Hospital, Texas A&M University, College Station, TX, 77843, USA

    I. Steele-Russell & M. I. Russell

  5. Department of Psychology, TAMU CVMBS, Texas A&M University, College Station, TX, 77843, USA

    B. Setlow

  6. Department of Neurophysiology, The Nencki Institute of Experimental Biology, Warsaw, Poland

    T. Werka

Authors
  1. I. Steele-Russell
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  2. M. I. Russell
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  3. J. A. Castiglioni
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  4. B. Setlow
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  5. T. Werka
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Corresponding author

Correspondence to I. Steele-Russell.

Additional information

This research was supported by S&W research grants ID# 1810 to ISR and ID# 7985 to JAC.

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Steele-Russell, I., Russell, M.I., Castiglioni, J.A. et al. The role of sensory pathways in Pavlovian conditioning in rabbit. Exp Brain Res 185, 199–213 (2008). https://doi.org/10.1007/s00221-007-1144-4

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