Sound recognition and localization in man: specialized cortical networks and effects of acute circumscribed lesions

• Published in: Experimental brain research Vol. 153; no. 4; pp. 591 - 604
• Main Authors: Adriani, Michela, Maeder, Philippe, Meuli, Reto, Thiran, Anne Bellmann, Frischknecht, Rolf, Villemure, Jean-Guy, Mayer, James, Annoni, Jean-Marie, Bogousslavsky, Julien, Fornari, Eleonora, Thiran, Jean-Philippe, Clarke, Stephanie
• Format: Journal Article Conference Proceeding
• Language: English
• Published: Berlin Springer 01.12.2003; Springer Nature B.V
• Subjects: Acute Disease; Adolescent; Adult; Aged; Auditory Perception - physiology; Biological and medical sciences; Brain Mapping; Cerebral Cortex - pathology; Cerebral Cortex - physiopathology; Cerebral Infarction - pathology; Cerebral Infarction - physiopathology; Cerebral Infarction - psychology; Ear and associated structures. Auditory pathways and centers. Hearing. Vocal organ. Phonation. Sound production. Echolocation; Female; Functional Laterality - physiology; Fundamental and applied biological sciences. Psychology; Humans; Language Development Disorders - pathology; Language Development Disorders - physiopathology; Language Development Disorders - psychology; Localization; Magnetic Resonance Imaging; Male; Middle Aged; Models, Neurological; Motion Perception - physiology; Nerve Net - pathology; Nerve Net - physiopathology; Neural Pathways - pathology; Neural Pathways - physiopathology; Neuropsychological Tests; Patients; Sound; Sound Localization - physiology; Time Factors; Vertebrates: nervous system and sense organs; Human; Stimulus localization; Functional organization; Central nervous system; Cortex; Auditory cortex; Encephalon; Hearing; Auditory; Nervous network; Plasticity; Information processing; Parallel processing; Auditory pathway; Diaschisis
• ISSN: 0014-4819; 1432-1106
• DOI: 10.1007/s00221-003-1616-0

Functional imaging studies have shown that information relevant to sound recognition and sound localization are processed in anatomically distinct cortical networks. We have investigated the functional organization of these specialized networks by evaluating acute effects of circumscribed hemispheric lesions. Thirty patients with a primary unilateral hemispheric lesion, 15 with right-hemispheric damage (RHD) and 15 with left-hemispheric damage (LHD), were evaluated for their capacity to recognise environmental sounds, to localize sounds in space and to perceive sound motion. One patient with RHD and 2 with LHD had a selective deficit in sound recognition; 3 with RHD a selective deficit in sound localization; 2 with LHD a selective deficit in sound motion perception; 4 with RHD and 3 with LHD a combined deficit of sound localization and motion perception; 2 with RHD and 1 with LHD a combined deficit of sound recognition and motion perception; and 1 with LHD a combined deficit of sound recognition, localization and motion perception. Five patients with RHD and 6 with LHD had normal performance in all three domains. Deficient performance in sound recognition, sound localization and/or sound motion perception was always associated with a lesion that involved the shared auditory structures and the specialized What and/or Where networks, while normal performance was associated with lesions within or outside these territories. Thus, damage to regions known to be involved in auditory processing in normal subjects is necessary, but not sufficient for a deficit to occur. Lesions of a specialized network was not always associated with the corresponding deficit. Conversely, specific deficits tended not be associated predominantly with lesions of the corresponding network; e.g. deficits in auditory spatial tasks were observed in patients whose lesions involved to a larger extent the shared auditory structures and the specialized What network than the specialized Where network, and deficits in sound recognition in patients whose lesions involved mostly the shared auditory structures and to a varying degree the specialized What network. The human auditory cortex consists of functionally defined auditory areas, whose intrinsic organization is currently not understood. In particular, areas involved in the What and Where pathways can be conceived as: (1) specialized regions, in which lesions cause dysfunction limited to the damaged part; observed deficits should be then related to the specialization of the damaged region and their magnitude to the extent of the damage; or (2) specialized networks, in which lesions cause dysfunction that may spread over the two specialized networks; observed deficits may then not be related to the damaged region and their magnitude not proportional to the extent of the damage. Our results support strongly the network hypothesis.