Decoding Visual Location From Neural Patterns in the Auditory Cortex of the Congenitally Deaf

Abstract

Sensory cortices of individuals who are congenitally deprived of a sense can exhibit considerable plasticity and be recruited to process information from the senses that remain intact. Here, we explored whether the auditory cortex of congenitally deaf individuals represents visual field location of a stimulus—a dimension that is represented in early visual areas. We used functional MRI to measure neural activity in auditory and visual cortices of congenitally deaf and hearing humans while they observed stimuli typically used for mapping visual field preferences in visual cortex. We found that the location of a visual stimulus can be successfully decoded from the patterns of neural activity in auditory cortex of congenitally deaf but not hearing individuals. This is particularly true for locations within the horizontal plane and within peripheral vision. These data show that the representations stored within neuroplastically changed auditory cortex can align with dimensions that are typically represented in visual cortex.

Keywords

neuroplasticity congenital deafness visual location sensory reorganization fMRI multivariate pattern analysis decoding

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References

Barone

Lacassagne

Kral

(2013). Reorganization of the connectivity of cortical field DZ in congenitally deaf cat. PLoS ONE, 8(4), Article e60093. doi:10.1371/journal.pone.0060093

Bavelier

Neville

(2002). Cross-modal plasticity: Where and how? Nature Reviews Neuroscience, 3, 443–452.

Bavelier

Tomann

Hutton

Mitchell

Corina

Liu

Neville

(2000). Visual attention to the periphery is enhanced in congenitally deaf individuals. The Journal of Neuroscience, 20, 1–6.

Bosworth

R. G.

Dobkins

K. R.

(2002). Visual field asymmetries for motion processing in deaf and hearing signers. Brain and Cognition, 49, 170–181.

Brainard

M. S.

Knudsen

E. I.

(1993). Experience-dependent plasticity in the inferior colliculus: A site for visual calibration of the neural representation of auditory space in the barn owl. The Journal of Neuroscience, 13, 4589–4608.

Chang

C.-C.

Lin

C.-J.

(2014). LIBSVM—A library for support vector machines (Version 3.20) [Computer software]. Retrieved from http://www.csie.ntu.edu.tw/~cjlin/libsvm/

Da Costa

van der Zwaag

Marques

J. P.

Frackowiak

R. S.

Clarke

Saenz

(2011). Human primary auditory cortex follows the shape of Heschl’s gyrus. The Journal of Neuroscience, 31, 14067–14075.

Fine

Finney

E. M.

Boynton

G. M.

Dobkins

K. R.

(2005). Comparing the effects of auditory deprivation and sign language within the auditory and visual cortex. Journal of Cognitive Neuroscience, 17, 1621–1637.

Finney

E. M.

Fine

Dobkins

K. R.

(2001). Visual stimuli activate auditory cortex in the deaf. Nature Neuroscience, 4, 1171–1173.

10.

Ghazanfar

A. A.

Schroeder

C. E.

(2006). Is neocortex essentially multisensory? Trends in Cognitive Sciences, 10, 278–285.

11.

Goebel

Esposito

Formisano

(2006). Analysis of functional image analysis contest (FIAC) data with BrainVoyager QX: From single-subject to cortically aligned group general linear model analysis and self-organizing group independent component analysis. Human Brain Mapping, 27, 392–401.

12.

Gougoux

Lepore

Lassonde

Voss

Zatorre

R. J.

Belin

(2004). Neuropsychology: Pitch discrimination in the early blind. Nature, 430, 309.

13.

Haxby

J. V.

Gobbini

M. I.

Furey

M. L.

Ishai

Schouten

J. L.

Pietrini

(2001). Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science, 293, 2425–2430.

14.

Haxby

J. V.

Guntupalli

J. S.

Connolly

A. C.

Halchenko

Y. O.

Conroy

B. R.

Gobbini

M. I.

. . . Ramadge

P. J.

(2011). A common, high-dimensional model of the representational space in human ventral temporal cortex. Neuron, 72, 404–416.

15.

Hickok

Poeppel

Clark

Buxton

R. B.

Rowley

H. A.

Roberts

T. P.

(1997). Sensory mapping in a congenitally deaf subject: MEG and fMRI studies of cross-modal non-plasticity. Human Brain Mapping, 5, 437–444.

16.

Hunt

D. L.

Yamoah

E. N.

Krubitzer

(2006). Multisensory plasticity in congenitally deaf mice: How are cortical areas functionally specified? Neuroscience, 139, 1507–1524.

17.

Karns

C. M.

Dow

M. W.

Neville

H. J.

(2012). Altered cross-modal processing in the primary auditory cortex of congenitally deaf adults: A visual-somatosensory fMRI study with a double-flash illusion. The Journal of Neuroscience, 32, 9626–9638.

18.

Kral

Schröder

J. H.

Klinke

Engel

A. K.

(2003). Absence of cross-modal reorganization in the primary auditory cortex of congenitally deaf cats. Experimental Brain Research, 153, 605–613.

19.

Kriegeskorte

Goebel

Bandettini

(2006). Information-based functional brain mapping. Proceedings of the National Academy of Sciences, USA, 103, 3863–3868.

20.

Levänen

Hamdorf

(2001). Feeling vibrations: Enhanced tactile sensitivity in congenitally deaf humans. Neuroscience Letters, 301, 75–77.

21.

Levänen

Jousmäki

Hari

(1998). Vibration-induced auditory-cortex activation in a congenitally deaf adult. Current Biology, 8, 869–872.

22.

Lomber

S. G.

Meredith

M. A.

Kral

(2010). Crossmodal plasticity in specific auditory cortices underlies visual compensations in the deaf. Nature Neuroscience, 13, 1421–1427.

23.

Meredith

M. A.

Kryklywy

McMillan

A. J.

Malhotra

Lum-Tai

Lomber

S. G.

(2011). Crossmodal reorganization in the early deaf switches sensory, but not behavioral roles of auditory cortex. Proceedings of the National Academy of Sciences, USA, 108, 8856–8861.

24.

Meredith

M. A.

Lomber

S. G.

(2011). Somatosensory and visual crossmodal plasticity in the anterior auditory field of early-deaf cats. Hearing Research, 280, 38–47.

25.

Meyer

Kaplan

J. T.

Essex

Webber

Damasio

(2010). Predicting visual stimuli on the basis of activity in auditory cortices. Nature Neuroscience, 13, 667–668.

26.

Neville

H. J.

Lawson

(1987a). Attention to central and peripheral visual space in a movement detection task: An event-related potential and behavioral study. II. Congenitally deaf adults. Brain Research, 405, 268–283.

27.

Neville

H. J.

Lawson

(1987b). Attention to central and peripheral visual space in a movement detection task: An event-related potential and behavioral study. III. Separate effects of auditory deprivation and acquisition of a visual language. Brain Research, 405, 284–294.

28.

Nishimura

Hashikawa

Doi

Iwaki

Watanabe

Kusuoka

. . . Kubo

(1999). Sign language ‘heard’ in the auditory cortex. Nature, 397, 116.

29.

Penhune

V. B.

Zatorre

R. J.

MacDonald

J. D.

Evans

A. C.

(1996). Interhemispheric anatomical differences in human primary auditory cortex: Probabilistic mapping and volume measurement from magnetic resonance scans. Cerebral Cortex, 6, 661–672.

30.

Rajan

Aitkin

L. M.

Irvine

D. R.

(1990). Azimuthal sensitivity of neurons in primary auditory cortex of cats. II. Organization along frequency-band strips. Journal of Neurophysiology, 64, 888–902.

31.

Reynolds

H. N.

(1993). Effects of foveal stimulation on peripheral visual processing and laterality in deaf and hearing subjects. American Journal of Psychology, 106, 523–540.

32.

Roe

A. W.

Pallas

S. L.

Hahm

J. O.

Sur

(1990). A map of visual space induced in primary auditory cortex. Science, 250, 818–820.

33.

Sadato

Pascual-Leone

Grafman

Ibañez

Deiber

M. P.

Dold

Hallett

(1996). Activation of the primary visual cortex by Braille reading in blind subjects. Nature, 380, 526–528.

34.

Sandmann

Dillier

Eichele

Meyer

Kegel

Pascual-Marqui

R. D.

. . . Debener

(2012). Visual activation of auditory cortex reflects maladaptive plasticity in cochlear implant users. Brain, 135, 555–568.

35.

Schneider

K. A.

Richter

M. C.

Kastner

(2004). Retinotopic organization and functional subdivisions of the human lateral geniculate nucleus: A high-resolution functional magnetic resonance imaging study. The Journal of Neuroscience, 24, 8975–8985.

36.

Scott

G. D.

Karns

C. M.

Dow

M. W.

Stevens

Neville

H. J.

(2014). Enhanced peripheral visual processing in congenitally deaf humans is supported by multiple brain regions, including primary auditory cortex. Frontiers in Human Neuroscience, 8, Article 177. doi:10.3389/fnhum.2014.00177

37.

Sereno

M. I.

Dale

A. M.

Reppas

J. B.

Kwong

K. K.

Belliveau

J. W.

Brady

T. J.

. . . Tootell

R. B.

(1995). Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science, 268, 889–893.

38.

Shiell

M. M.

Champoux

Zatorre

R. J.

(2015). Reorganization of auditory cortex in early-deaf people: Functional connectivity and relationship to hearing aid use. Journal of Cognitive Neuroscience, 27, 150–163.

39.

Smith

A. M.

Lewis

B. K.

Ruttimann

U. E.

F. Q.

Sinnwell

T. M.

Yang

. . . Frank

J. A.

(1999). Investigation of low frequency drift in fMRI signal. NeuroImage, 9, 526–533.

40.

Talairach

Tournoux

(1988). Co-planar stereotaxic atlas of the human brain. New York, NY: Thieme.

41.

Van Boven

R. W.

Hamilton

R. H.

Kauffman

Keenan

J. P.

Pascual-Leone

(2000). Tactile spatial resolution in blind Braille readers. Neurology, 54, 2230–2236.

42.

Vetter

Smith

F. W.

Muckli

(2014). Decoding sound and imagery content in early visual cortex. Current Biology, 24, 1256–1262.

43.

Watanabe

Cheng

Murayama

Ueno

Asamizuya

Tanaka

Logothetis

(2011). Attention but not awareness modulates the BOLD signal in the human V1 during binocular suppression. Science, 334, 829–831.

44.

Watkins

K. E.

Shakespeare

T. J.

O’Donoghue

M. C.

Alexander

Ragge

Cowey

Bridge

(2013). Early auditory processing in area V5/MT+ of the congenitally blind brain. The Journal of Neuroscience, 33, 18242–18246.

45.

Wong

Chabot

Kok

M. A.

Lomber

S. G.

(2014). Modified areal cartography in auditory cortex following early- and late-onset deafness. Cerebral Cortex, 24, 1778–1792. doi:10.1093/cercor/bht026

46.

Zhang

Zhaoping

Zhou

Fang

(2012). Neural activities in V1 create a bottom-up saliency map. Neuron, 73, 183–192.

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