Tone deafness: a new disconnection syndrome?
Communicating with one's environment requires efficient neural interaction between action and perception. Neural substrates of sound perception and production are connected by the arcuate fasciculus (AF). Although AF is known to be involved in language, its roles in non-linguistic functions are unexplored. Here, we show that tone-deaf people, with impaired sound perception and production, have reduced AF connectivity. Diffusion tensor tractography and psychophysics were assessed in tone-deaf individuals and matched controls. Abnormally reduced AF connectivity was observed in the tone deaf. Furthermore, we observed relationships between AF and auditory-motor behavior: superior and inferior AF branches predict psychophysically assessed pitch discrimination and sound production perception abilities, respectively. This neural abnormality suggests that tone deafness leads to a reduction in connectivity resulting in pitch-related impairments. Results support a dual-stream anatomy of sound production and perception implicated in vocal communications. By identifying white matter differences and their psychophysical correlates, results contribute to our understanding of how neural connectivity subserves behavior.
Loui
Psyche
P
Department of Neurology and Radiology, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA 02215, USA. ploui@bidmc.harvard.edu
Alsop
David
D
Schlaug
Gottfried
G
D000161:Acoustic Stimulation / Q000379:methods; D000328:Adult; D001307:Auditory Perception / Q000502:physiology; D003638:Deafness / Q000145:classification* / Q000175:diagnosis / Q000503:physiopathology*; D005260:Female; D006801:Humans; D008297:Male; D008875:Middle Aged; D010897:Pitch Discrimination / Q000502:physiology*; D010898:Pitch Perception / Q000502:physiology; D011601:Psychophysics / Q000379:methods* / Q000639:trends; D013577:Syndrome
Curr Opin Neurol. 2006 Aug;19(4):379-85
16914977
Brain. 2006 Oct;129(Pt 10):2562-70
16931534
Brain. 2004 Apr;127(Pt 4):801-10
14985262
Curr Biol. 2008 May 6;18(9):R387-8
18460320
Neuron. 2002 Jan 17;33(2):185-91
11804567
Cortex. 2008 Sep;44(8):953-61
18614162
J Pediatr. 2008 Feb;152(2):250-5
18206698
Brain. 2005 Nov;128(Pt 11):2562-77
16049045
Cortex. 2008 Sep;44(8):936-52
18635164
Neuroimage. 2005 Feb 1;24(3):656-66
15652301
Neuroimage. 2008 Feb 1;39(3):1370-82
18024157
Brain. 2002 Feb;125(Pt 2):238-51
11844725
Ann Neurol. 1999 Feb;45(2):265-9
9989633
Arch Neurol. 2008 May;65(5):619-26
18474737
NMR Biomed. 1995 Nov-Dec;8(7-8):333-44
8739270
Ann Neurol. 2005 Sep;58(3):478-82
16130110
Neuron. 2007 Aug 2;55(3):521-32
17678862
Radiology. 2004 Jan;230(1):77-87
14645885
Curr Biol. 2008 Apr 22;18(8):R331-2
18430629
Brain Res Cogn Brain Res. 1996 Mar;3(2):131-41
8713554
Nat Neurosci. 2007 Jul;10(7):915-21
17589505
Neuroimage. 2007 Apr 15;35(3):1064-76
17320414
Brain. 2006 Jul;129(Pt 7):1822-32
16714319
Am J Psychiatry. 2007 Jul;164(7):1005
17606649
Trends Neurosci. 1992 Jan;15(1):20-5
1374953
Ann N Y Acad Sci. 2003 Nov;999:58-75
14681118
Cereb Cortex. 2008 Nov;18(11):2471-82
18281301
J Neurosci. 2007 Nov 21;27(47):13028-32
18032676
Brain Cogn. 2005 Dec;59(3):310-3
16337871
Neuroimage. 2008 Jan 1;39(1):62-79
17919935
IEEE Trans Med Imaging. 2007 Nov;26(11):1472-82
18041263
Magn Reson Med. 2000 Oct;44(4):625-32
11025519
Cognition. 2004 May-Jun;92(1-2):67-99
15037127
Neuroimage. 2008 Feb 1;39(3):1429-43
18035557
Nat Rev Neurosci. 2005 Jul;6(7):576-82
15959465
Ann N Y Acad Sci. 2005 Dec;1060:311-24
16597781
J Neurosci. 2007 Apr 4;27(14):3799-806
17409244
Magn Reson Med. 1999 Jul;42(1):37-41
10398948
Restor Neurol Neurosci. 2007;25(3-4):323-34
17943009
Cortex. 2005 Jun;41(3):354-63
15871600
Science. 2002 Aug 2;297(5582):846-8
12161656
Nat Rev Neurosci. 2007 May;8(5):393-402
17431404
Nat Neurosci. 2009 Jan;12(1):29-31
19029889
Ann N Y Acad Sci. 2009 Jul;1169:121-5
19673766
J Neurosci. 2007 Jan 10;27(2):308-14
17215391
Perspect Psychol Sci. 2009 May;4(3):274-90
26158964