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Goal-oriented searching mediated by ventral hippocampus early in trial-and-error learning

Nature Neuroscience volume 15, pages 1563–1571 (2012)Cite this article

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Abstract

Most behavioral learning in biology is trial and error, but how these learning processes are influenced by individual brain systems is poorly understood. Here we show that ventral-to-dorsal hippocampal subdivisions have specific and sequential functions in trial-and-error maze navigation, with ventral hippocampus (vH) mediating early task-specific goal-oriented searching. Although performance and strategy deployment progressed continuously at the population level, individual mice showed discrete learning phases, each characterized by particular search habits. Transitions in learning phases reflected feedforward inhibitory connectivity (FFI) growth occurring sequentially in ventral, then intermediate, then dorsal hippocampal subdivisions. FFI growth at vH occurred abruptly upon behavioral learning of goal-task relationships. vH lesions or the absence of vH FFI growth delayed early learning and disrupted performance consistency. Intermediate hippocampus lesions impaired intermediate place learning, whereas dorsal hippocampus lesions specifically disrupted late spatial learning. Trial-and-error navigational learning processes in naive mice thus involve a stereotype sequence of increasingly precise subtasks learned through distinct hippocampal subdivisions. Because of its unique connectivity, vH may relate specific goals to internal states in learning under healthy and pathological conditions.

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Figure 1: Sequential deployment of search-strategy habits during water maze learning.
Figure 2: Sequential recruitment of hippocampal subdivisions during maze learning.
Figure 3: Specific task-goal association reflected by vH FFI growth during maze learning.
Figure 4: Role of vH in water maze learning.
Figure 5: Function of iH in water maze learning.
Figure 6: Function of dH in water maze learning.
Figure 7: vH-dependent maze learning, independent of dH.

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Acknowledgements

We thank B. Sacchetti (University of Torino), C. Sandi (École Polytechnique Fédérale de Lausanne) and S. Arber (Friedrich Miescher Institut) for comments on the manuscript. The Friedrich Miescher Institut is part of the Novartis Research Foundation.

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  1. Sarah Ruediger, Dominique Spirig and Flavio Donato: These authors contributed equally to this work.

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  1. Friedrich Miescher Institute, Basel, Switzerland

    Sarah Ruediger, Dominique Spirig, Flavio Donato & Pico Caroni

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  1. Sarah Ruediger
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Contributions

S.R. devised and carried out the analysis of hippocampal behavior, connectivity, vH lesions and β-adducin rescue; D.S. carried out the analysis of FFI growth and c-Fos immunoreactivity; F.D. devised and carried out behavioral and lesion studies relating vH, iH and dH FFI growth to subdivision function in learning. P.C. helped devise the experiments and wrote the manuscript. All authors discussed the results and commented the manuscript.

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Correspondence to Pico Caroni.

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The authors declare no competing financial interests.

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Ruediger, S., Spirig, D., Donato, F. et al. Goal-oriented searching mediated by ventral hippocampus early in trial-and-error learning. Nat Neurosci 15, 1563–1571 (2012). https://doi.org/10.1038/nn.3224

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