Neuronal Plasticity and Multisensory Integration in Filial Imprinting

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2011 Mar 23

PMID 21423770

Citations 5

Authors

Stephen Michael Town

Brian John McCabe

Affiliations

Soon will be listed here.

Abstract

Many organisms sample their environment through multiple sensory systems and the integration of multisensory information enhances learning. However, the mechanisms underlying multisensory memory formation and their similarity to unisensory mechanisms remain unclear. Filial imprinting is one example in which experience is multisensory, and the mechanisms of unisensory neuronal plasticity are well established. We investigated the storage of audiovisual information through experience by comparing the activity of neurons in the intermediate and medial mesopallium of imprinted and naïve domestic chicks (Gallus gallus domesticus) in response to an audiovisual imprinting stimulus and novel object and their auditory and visual components. We find that imprinting enhanced the mean response magnitude of neurons to unisensory but not multisensory stimuli. Furthermore, imprinting enhanced responses to incongruent audiovisual stimuli comprised of mismatched auditory and visual components. Our results suggest that the effects of imprinting on the unisensory and multisensory responsiveness of IMM neurons differ and that IMM neurons may function to detect unexpected deviations from the audiovisual imprinting stimulus.

Citing Articles

Visual Imprinting in Birds: Behavior, Models, and Neural Mechanisms.

McCabe B Front Physiol. 2019; 10:658.

PMID: 31231236 PMC: 6558373. DOI: 10.3389/fphys.2019.00658.

Translational control of auditory imprinting and structural plasticity by eIF2α.

Batista G, Johnson J, Dominguez E, Costa-Mattioli M, Pena J Elife. 2016; 5.

PMID: 28009255 PMC: 5245967. DOI: 10.7554/eLife.17197.

Social Memory Formation Rapidly and Differentially Affects the Motivation and Performance of Vocal Communication Signals in the Bengalese Finch (Lonchura striata var. domestica).

Toccalino D, Sun H, Sakata J Front Behav Neurosci. 2016; 10:113.

PMID: 27378868 PMC: 4906024. DOI: 10.3389/fnbeh.2016.00113.

Perineuronal satellite neuroglia in the telencephalon of New Caledonian crows and other Passeriformes: evidence of satellite glial cells in the central nervous system of healthy birds?.

Medina F, Hunt G, Gray R, Wild J, Kubke M PeerJ. 2013; 1:e110.

PMID: 23904989 PMC: 3728766. DOI: 10.7717/peerj.110.

The effects of social rearing on preferences formed during filial imprinting and their neural correlates.

Town S Exp Brain Res. 2011; 212(4):575-81.

PMID: 21688140 DOI: 10.1007/s00221-011-2769-x.

References

Gray C, Maldonado P, Wilson M, McNaughton B . Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex. J Neurosci Methods. 1995; 63(1-2):43-54. DOI: 10.1016/0165-0270(95)00085-2. View

Ghazanfar A, Schroeder C . Is neocortex essentially multisensory?. Trends Cogn Sci. 2006; 10(6):278-85. DOI: 10.1016/j.tics.2006.04.008. View

Horn G, Nicol A, Brown M . Tracking memory's trace. Proc Natl Acad Sci U S A. 2001; 98(9):5282-7. PMC: 33201. DOI: 10.1073/pnas.091094798. View

McCabe B, Horn G, Kendrick K . GABA, taurine and learning: release of amino acids from slices of chick brain following filial imprinting. Neuroscience. 2001; 105(2):317-24. DOI: 10.1016/s0306-4522(01)00186-5. View

Taylor A, SLUCKIN W, Hewitt R, Guiton P . The formation of attachments by domestic chicks to two textures. Anim Behav. 1967; 15(4):514-9. DOI: 10.1016/0003-3472(67)90052-8. View

Ernst M, Bulthoff H . Merging the senses into a robust percept. Trends Cogn Sci. 2004; 8(4):162-9. DOI: 10.1016/j.tics.2004.02.002. View

Naumer M, Doehrmann O, Muller N, Muckli L, Kaiser J, Hein G . Cortical plasticity of audio-visual object representations. Cereb Cortex. 2008; 19(7):1641-53. PMC: 2693620. DOI: 10.1093/cercor/bhn200. View

Horn G . Pathways of the past: the imprint of memory. Nat Rev Neurosci. 2004; 5(2):108-20. DOI: 10.1038/nrn1324. View

Bradley P, Davies D, Horn G . Connections of the hyperstriatum ventrale of the domestic chick (Gallus domesticus). J Anat. 1985; 140 ( Pt 4):577-89. PMC: 1165083. View

10.

Lewicki M . A review of methods for spike sorting: the detection and classification of neural action potentials. Network. 1999; 9(4):R53-78. View

11.

Xiang J, Brown M . Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe. Neuropharmacology. 1998; 37(4-5):657-76. DOI: 10.1016/s0028-3908(98)00030-6. View

12.

Nicol A, Brown M, Horn G . Neurophysiological investigations of a recognition memory system for imprinting in the domestic chick. Eur J Neurosci. 1995; 7(4):766-76. DOI: 10.1111/j.1460-9568.1995.tb00680.x. View

13.

Shams L, Seitz A . Benefits of multisensory learning. Trends Cogn Sci. 2008; 12(11):411-7. DOI: 10.1016/j.tics.2008.07.006. View

14.

Kim R, Seitz A, Shams L . Benefits of stimulus congruency for multisensory facilitation of visual learning. PLoS One. 2008; 3(1):e1532. PMC: 2211398. DOI: 10.1371/journal.pone.0001532. View

15.

Kayser C, Logothetis N, Panzeri S . Visual enhancement of the information representation in auditory cortex. Curr Biol. 2009; 20(1):19-24. DOI: 10.1016/j.cub.2009.10.068. View

16.

Davies D, Horn G, McCabe B . Changes in telencephalic catecholamine levels in the domestic chick. Effects of age and visual experience. Brain Res. 1983; 312(2):251-5. DOI: 10.1016/0165-3806(83)90141-4. View

17.

Tanabe H, Honda M, Sadato N . Functionally segregated neural substrates for arbitrary audiovisual paired-association learning. J Neurosci. 2005; 25(27):6409-18. PMC: 6725270. DOI: 10.1523/JNEUROSCI.0636-05.2005. View

18.

McCabe B, Horn G, BATESON P . Effects of restricted lesions of the chick forebrain on the acquisition of filial preferences during imprinting. Brain Res. 1981; 205(1):29-37. DOI: 10.1016/0006-8993(81)90717-4. View

19.

Jackson C, McCabe B, Nicol A, Grout A, Brown M, Horn G . Dynamics of a memory trace: effects of sleep on consolidation. Curr Biol. 2008; 18(6):393-400. DOI: 10.1016/j.cub.2008.01.062. View

20.

Meredith M, Stein B . Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. J Neurophysiol. 1986; 56(3):640-62. DOI: 10.1152/jn.1986.56.3.640. View