Also see the archival list of Science's Compass: Enhanced Perspectives
Michael P. Stryker*
Enhanced: Sensory Maps on the Move
Many features of the world are represented in the brain as orderly maps [HN1].
These maps can show remarkable plasticity, undergoing reorganization
after brain damage or changes in sensory stimulation. In some cases,
the maps may even shift so that stimuli activating one group of neurons
now activate a completely different set of neurons. The report by Zheng
and Knudsen [HN2] on page 962 of this issue (1) offers new insight into how brain maps move. These investigators analyzed how the auditory space map of young barn owls [HN3]
changes in response to alterations in the visual space map. (The
auditory and visual space maps of barn owls are closely connected so
that the birds, which cannot rotate their eyes, are able to precisely
locate their prey [HN4] using either hearing or
sight.) In previous work the authors demonstrated that a newly learned
auditory map requires the formation of new excitatory connections. Now
they show that the excitatory inputs for the old and new auditory maps
coexist but that excitation from the old map is selectively overwhelmed
by inhibition from GABA-containing neurons [HN5].
These results raise new questions about the specification and control
of inhibitory connections in the brain and the critical periods for
neural plasticity during animal development.
The Knudsen and Konishi [HN6] laboratories have spent many years describing the neural circuits that control auditory localization in the barn owl [HN7] (2).
Unlike visual or tactile space maps, the auditory space map must be
constructed by the brain in the external nucleus of the inferior
colliculus (Icx) [HN8]. Neurons in the ear
respond in the same way to a sound of a particular frequency and
intensity no matter where the sound comes from. The brain constructs
the auditory space map by comparing the responses of neurons in the two
ears to a sound that stimulates both. Left-right positioning of the
sound source is computed from the different arrival times of the sound
at each ear.
The computation is subtle because the actual time at which a sound
begins is not known to the brain, and most auditory neurons are tuned
to respond to tones of air pressure of a particular frequency. The
sound waves from a source that is straight ahead arrive at the two ears
at the same moment. But if the sound source of a particular frequency
is displaced so that it is exactly one wavelength nearer to or farther
from one ear than the other, the sounds reaching the ears are very
similar to the sound arriving from straight ahead. Thus, there is an
ambiguity about the localization of pure-tone stimuli. The brain
resolves this ambiguity by combining information from neurons that are
selective for different frequencies of sound. The signal in each neuron
is ambiguous, but only one position of the sound source will be
consistent with all of these ambiguities when examined in combination (3).
This combination occurs through connections from neurons in the central
nucleus of the inferior colliculus (ICc)--which is tonotopically
organized according to sound frequency--to neurons in the ICx--which is
organized according to left-right positioning encoded by differences in
arrival times (see the figure). The inferior colliculus neurons send
their main output to the optic tectum [HN9] and
activate neurons that are also driven by visual stimulation from the
same point in space as the sound source. Thus, either the sight or the
sound of the mouse can stimulate the owl to the same action, turning
toward its prey.
Maps of sound and light. The auditory and visual space
maps of barn owls are connected, enabling the birds to precisely locate
prey. The sight of the mouse stimulates retinal neurons to send signals
to activate part of the optic tectum, which orients the owl toward its
prey. The sound of the mouse stimulates the two ears with a particular
interaural time difference, to which certain neurons in the ICx are
sensitive. (These neurons receive input from the ICc at conventional
AMPA receptors, A). The ICx neurons activate the same region of the
optic tectum as visual stimuli. In juvenile owls reared in prism
spectacles that alter the visual space map, the ICc makes new
excitatory connections (through NMDA receptors, N) to the ICx.
Excitatory signals from the old connections are overcome by a selective
increase in inhibition from GABA-containing neurons, G). Thus, the
sound and sight of the mouse again cause orientation to the same
Zheng and Knudsen (1) reared young owls in prism spectacles [HN10]
that displaced the visual image of the world to the left or right. If
the owls wear these spectacles during a critical period in early life,
they learn to compensate and regain the ability to accurately locate
prey. The compensation takes place in the auditory space map of the
ICx, which changes to become consistent with the visual map. Earlier
work showed that the changes in the auditory space map are partly
attributable to the growth of new excitatory inputs from the ICc to the
ICx (4). These new neural connections respond to the excitatory neurotransmitter glutamate through synaptic membrane NMDA (N-methyl-D-aspartate) receptors [HN11] (5).
New excitatory connections explain how neurons in the ICx respond to
the appropriate position in space dictated by the altered visual map.
But why do the ICx neurons stop responding to the old position? It
turns out that the old excitatory inputs remain, but the ICx neurons
now receive strong inhibitory input that is activated by the same
auditory stimuli that activated the original excitatory connections.
The inhibition sums with the excitation so that the ICx neurons no
longer respond to the old stimuli. For the cells of the optic tectum
that "listen" to the ICx neurons, the new auditory field appears
similar in kind to the old one, but is just located in a different
place. The neural circuitry that maintains the relocated receptive
field is, however, quite different.
These findings explain why the normal auditory space map is restored in
owls when the prism spectacles are removed, even at an age when normal
owls have lost the ability to adapt to a rearranged visual map (4).
The original neural circuitry is still there, and all that is needed
for it to assume control is removal of inhibitory input. Inhibitory
connections also explain why the capacity for plasticity in adult owls
is greater if they have adapted to rearranged maps as juveniles (6).
What rule of neural plasticity [HN12]
regulates the strength of these inhibitory connections? Inhibition is
selectively increased for those positions in space that receive strong
excitatory input but do not match the position at which ICx neurons
target cells in the optic tectum. Such a rule requires that a
retrograde signal travels from the tectal cells to the axonal terminals
of the ICx cells and thence to their cell bodies and dendrites, where
it enhances responses to inhibitory inputs at GABA receptors. These
dual contingencies show that inhibitory connections are weakened under
circumstances in which excitatory connections are strengthened and vice
versa (7). Such a reciprocal relationship between
the excitatory and inhibitory inputs makes sense, although as yet has
not been rigorously demonstrated.
How applicable are the new findings to the plasticity of other types of
sensory maps? There is little evidence for selective inhibition as the
mechanism of plasticity in the adult cortex--most long-range
connections are excitatory not inhibitory. However, a combination of
excitatory and inhibitory pathways may explain cases in which receptive
fields move, for example, after denervation of a digit or of two
adjacent digits (8).
In contrast, experiments in the visual cortex show that the loss of
response to the occluded eye after brief monocular deprivation is not
the consequence of selective inhibition from deprived-eye pathways (9). Nonetheless, appropriate inhibition is essential for normal plasticity in the visual cortex (10).
In the brain, as in life, it is not just what you do that matters, it's
also what you don't do. The plasticity of auditory spatial
representation in the owl brain depends not only on new excitatory
connections but also on overwhelming the persistent old connections
through inhibition. By combining and overlaying different plasticity
mechanisms in the auditory pathway, the owl is able to adjust its
various sensory maps so that they are in harmony.
- W. Zheng and E. I. Knudsen, Science 284, 962 (1999).
- M. Konishi, Harvey Lect. 86, 47 (1991); E. I. Knudsen, in Fundamental Neuroscience (Academic Press, 1999), pp. 637-654 [publisher's information].
- H. Wagner, T. Takahashi, M. Konishi, J. Neurosci. 7, 3105 (1987) [Medline]; K. Saberi et al., Proc. Natl. Acad. Sci. U.S.A. 95, 6465 (1998) [Medline].
- D. E. Feldman et al., J. Neurosci., 17, 6820 (1997) [Medline].
- D. E. Feldman, M. S. Brainard, E. I. Knudsen, Science 271, 525 (1996).
- E. I. Knudsen, ibid. 279, 1531 (1998).
- L. C. Rutherford et al., Neuron 21, 521 (1998) [Medline].
- M. M. Merzenich et al., Cold Spring Harb. Symp. Quant. Biol. 55, 873 (1990) [Medline].
- A. M. Sillito et al., Nature 291, 318 (1981) [Medline].
- T. K. Hensch et al., Science 282, 1504 (1998).
The author [HN13] is at the
Keck Center for Integrative Neuroscience, Department of Physiology,
University of California, San Francisco, CA 94143-0444, USA. E-mail: firstname.lastname@example.org
Related Resources on the World Wide Web
Neuroscience on the Internet is a searchable and browsable index of neuroscience resources available on the Internet.
WWW Virtual Library of Neuroscience is maintained by the
Department of Neurology and Neuroscience, Cornell University Medical College.
Center for the Neural Basis of Cognition provides links to
Cognitive-Neurosciences Resources on the Web.
neuroscience glossary is provided for a course on
computational neuroscience at the University of Wisconsin.
exploration of the nervous system is offered by E. Chudler of the University of Washington on his
Neuroscience for Kids Web site. His home page features an extensive list of
links to neuroscience Web resources.
Howard Hughes Medical Institute (HHMI) offers an illustrated
research report for the general reader titled "Seeing, hearing, and smelling the world."
- R. M. Robertson, Department of Biology, Queen's University, Kingston, Canada, provides extensive
lecture notes for a
course on integrative neurobiology and neuroethology.
P. Lennie, Center for Visual Science, University of Rochester, provides lecture notes for a
course on sensory systems.
Neuroscience Tutorial from the Washington University School of Medicine has sections on the
central visual pathways and the
summary report of a
workshop, held in December 1997 in Breckenridge, CO, on the neurophysiology of central auditory processing is presented by
C. deCharms, Keck Center for Integrative Neuroscience, University of California, San Francisco.
Neuroethology of Barn Owl Sound Localization is a Web site prepared by J. Wen as a class project for a
course on neural systems and animal behavior at Cornell University.
overview of brain organization and neural connections is provided in the
Brief Tour of the Brain from Syracuse University's
Mind and Machine Module project.
neurobiology laboratory course from the Division of Life Sciences, University of Texas, San Antonio, includes a presentation on
sensory processing that includes a discussion of sensory maps in the brain.
The HHMI presentation on the senses includes a discussion of sensory processing in the brain.
R. M. Robertson provides
lecture notes titled "Maps, columns, blobs, stripes and barrels."
W. Zheng and
E. Knudsen are in the
Department of Neurobiology, Stanford University School of Medicine; the faculty research directory also provides an
The Stanford University Medical Center Office of Communications issued
press releases about Knudsen's research with barn owls on
2 October 1996 about research published in the 3 October 1996 issue of Nature and on
5 March 1998 about research published in the 6 March 1998 issue of Science (6).
Peterson Online Birds has an entry for the
Natural Histories of Raptors
Web site from the Southeastern Raptor Rehabilitation Center, Auburn
University College of Veterinary Medicine, provides information about
Owl Pages presents photos and basic information about the
Web presentation on sound localization in the barn owl, J. Wen provides information on the
phylogeny and the
zoology of the barn owl.
introduction to auditory and visual localization in the barn owl is included in a
by A. Haessly, J. Sirosh, and R. Miikkulainen titled "A model of
visually guided plasticity of the auditory spatial map in the barn
owl," which was presented at the 1995 annual conference of the
Cognitive Science Society. G. Jacobs, Center for Computational Biology,
Montana State University, Bozeman, provides
lecture notes on visual calibration of sound localization in barn owls for a
course in neuroethology.
inhibitory synapse are defined in the
On-line Medical Dictionary.
THCME Medical Biochemistry Page provides information about
GABA in the section on
biochemistry of nerve transmission.
M. Konishi is in the Division of Biology, California Institute of Technology.
HHMI presentation on the senses includes a description of
Konishi's research on the auditory system of barn owls.
J. Wen's Web site provides an overview of
Konishi's early research on sound localization in barn owls.
Topics In Neuroethology: Model Systems page that was developed for a graduate seminar at the Beckman Institute, University of Illinois, presents a
citation analysis of the 19 May 1978 article in Science by Knudsen and Konishi titled "A neural map of auditory space in the owl."
G. Jacobs, Center for Computational Biology, Montana State, University, Bozeman, provides
lecture notes (in Adobe Acrobat format) on sound localization in barn owls for a
course in animal physiology.
Neuroethology of Barn Owl Sound Localization Web site, J. Wen includes a
presentation on the neural mechanism underlying the barn owl's sound localization.
P. Lennie offers lecture notes on
sound localization for a
course on sensory systems.
C. Carr, Department of Biology, University of Maryland, discusses the
midbrain and the inferior colliculus in lecture notes on hearing.
D. Atkins, Department of Biological Sciences, George Washington University, Washington, DC,
provides an introduction to the
lecture notes for a neurobiology course.
illustration from an
introduction to neuroanatomy, presented by the
Institute for Neurology and Neurosurgery, Beth Israel Hospital, NY, shows the location of the inferior colliculi in the human brain.
NeuroNames has an
entry for the central nucleus of the inferior colliculus with a link to an
illustration of its location in the macaque brain.
On-line Medical Dictionary defines
A photo of an
owl in prism spectacles is displayed in the
HHNI presentation titled "The value of having two ears."
NMDA receptor are defined in the
neuroscience glossary from the University of Wisconsin.
The On-line Medical Dictionary defines
excitatory amino acid.
HotMolecBase from the Bioinformatics Unit, Weizmann Institute of Science, Israel, has an entry for the
Exploring the Nervous System includes an
introduction to neurotransmitters and neuroactive peptides.
L. Clothier, Department of Psychiatry, University of Arkansas for Medical Sciences, presents overviews of
synaptic biology and
neurotransmitter systems in
lecture notes for a
course on behavioral sciences.
course on the biopsychology of learning and memory, S. Grossman, Department of Psychology, University of Chicago, offers a
Web lecture titled "Transfer of information between neurons," which includes a discussion of inhibitory and excitatory neurotransmitters.
news article in the Spring 1996 issue of
Stanford Medicine describes D. Feldman and E. Knudsen's research on NMDA receptors and owl neurons.
Dictionary of Cell Biology defines
Web edition of the forthcoming
MIT Encyclopedia of the Cognitive Sciences includes articles on
neural plasticity and
G. Wallis discusses
neural plasticity in his
D.Phil thesis titled "Neural mechanisms underlying processing in the visual areas of the occipital and temporal lobes."
Winter 1995 newsletter of the Neuroscience Research Center, University of Texas, Houston, had an
article by P. Kelly titled "Mechanisms regulating synaptic plasticity in brain."
Society for Neuroscience includes an article on
brain reorganization in its
Brain Briefings collection.
R. M. Robertson discusses synaptic plasticity in
lecture notes on learning and memory for a course in integrative neurobiology.
M. P. Stryker is in the
Department of Physiology, University of California, San Francisco.
Issue of 7 May 1999,
Copyright © 1999 by The American Association for the Advancement of Science. All rights reserved.