Right hemisphere specialization for intensity discrimination of musical and speech sounds

Abstract

Sound intensity is the primary and most elementary feature of auditory signals. Its discrimination plays a fundamental role in different behaviours related to auditory perception such as sound source localization, motion detection, and recognition of speech sounds. This study was aimed at investigating hemispheric asymmetries for processing intensity of complex tones and consonant-vowel syllables. Forty-four right-handed non-musicians were presented with two dichotic matching-to-sample tests with focused attention: one with complex tones of different intensities (musical test) and the other with consonant-vowel syllables of different intensities (speech test). Intensity differences (60, 70, and 80 dBA) were obtained by altering the gain of a synthesized harmonic tone (260 Hz fundamental frequency) and of a consonant-vowel syllable (/ba/) recorded from a natural voice. Dependent variables were accuracy and reaction time. Results showed a significant clear-cut left ear advantage in both tests for both dependent variables. A monaural control experiment ruled out possible attentional biases. This study provides behavioural evidence of a right hemisphere specialization for the perception of the intensity of musical and speech sounds in healthy subjects.

Introduction

Sound intensity is probably the primary and most elementary feature of auditory signals. It conveys key information about the strength and the distance of the sound source from the listener. Moreover, the discrimination of sound intensity has a basic role in many auditory functions such as recognition of environmental, musical, and speech sounds including non-verbal aspects of language, i.e. speech prosody (Brungart & Scott, 2001; Mitchell, Elliott, Barry, Cruttenden, & Woodruff, 2003; Trainor &Adams, 2000). Despite this, until now only few studies have investigated the neural mechanisms and hemispheric asymmetries underlying the perception of sound intensity (Belin et al., 1998; Jancke, Shah, Posse, Grosse-Ryuken, & Muller-Gartner, 1998; Paus et al., 1997; Wexler & Halwes, 1981). Conversely, many scientific reports based on behavioural and patients evidence have focused on the study of more complex aspects of auditory sensation. These studies have shown that a right hemisphere specialization can be demonstrated for the perception of pitch (Gregory, 1982; Paquette, Bourassa, & Peretz, 1996; Zatorre, 2001), timbre (Boucher & Bryden, 1997; Brancucci and San Martini, 1999, Brancucci and San Martini, 2003; Samson & Zatorre, 1994; Samson, Zatorre, & Ramsay, 2002) and other aspects (Boucher & Bryden, 1997; Schnider, Benson, Alexander, & Schnider-Klaus, 1994) of musical or environmental sounds, whereas auditory perception of speech stimuli is mainly left lateralized (Berlin, Lowe-Bell, Cullen, & Thompson, 1973; Hugdahl, 2000; Wernicke, 1874).

These findings have received support from neuroimaging studies. The earliest neuroimaging-based evidence for lateralized auditory functions was the one reported by Mazziotta, Phelps, Carson, and Kuhl (1982), using positron emission tomography. They presented their subjects with monaural and binaural verbal and non-verbal sounds, and found enhanced and more widespread blood flow in the left hemisphere for verbal sounds and in the right hemisphere for non-verbal sounds. After this study, other researchers using different neuroimaging and investigation methods, have given further sustain to the dichotomy verbal sounds/left hemisphere (Epstein, 1998; Ghazanfar & Hauser, 1999; Tranel, 1992) versus musical (or non-verbal) sounds/right hemisphere (Halpern, 2001, Milner, 1962; Tramo & Bharucha, 1991). There is general agreement on the fact that this dichotomy is based on a specialization of the left hemisphere in the analysis of fine temporal features of sound (Carmon & Nachshon, 1981; Efron, 1963, Kester et al., 1991; Zatorre & Belin, 2001; Zatorre, Belin, & Penhune, 2002), and on a specialization of the right hemisphere in the frequency analysis of the stimulus (Brancucci & San Martini, 2003; Greenwald & Jerger, 2003; Zatorre & Belin, 2001; Zatorre et al., 2002). Other alternative explanations are based on attentional factors (Geffen, 1988, Hugdahl et al., 2000), cognitive strategies (Mazziotta et al., 1982) and task demands (Greenwald & Jerger, 2003; Zatorre et al., 2002).

The present study uses dichotic listening with focused attention (Asbjornsen & Hugdahl, 1995; Hugdahl, 2000; Jancke, Specht, Shah, & Hugdahl, 2003) to investigate possible hemispheric asymmetries for the discrimination of sound intensity. Dichotic listening, meaning listening to two different auditory stimuli presented concomitantly one in the left and one in the right ear, is a classical neuropsychophysiological technique that has been broadly used for the study of laterality. It allows testing the two hemispheres separately as, when the two auditory pathways convey incongruent information to the auditory cortices, the ipsilateral pathway is suppressed thus allowing only the contralateral stimulus reaching the auditory cortex (Brancucci et al., 2004, Kimura, 1967). In this particular situation, testing the right ear means, with good approximation, testing the left auditory cortex and testing the left ear means testing the right auditory cortex (Hugdahl, 1995, Hugdahl et al., 1999). Functional magnetic resonance imaging studies on dichotic listening of consonant-vowel syllables have shown that brain activations during this task are dependent on attentional constraints and involve a highly distributed processing network, which extends from temporal lobe to superior temporal gyrus, middle and inferior frontal gyrus, cingulate cortex, and to higher order areas such as prefrontal regions (Jancke & Shah, 2002; Pollmann, Lepsien, Hugdahl, & von Cramon, 2004; Thomsen, Rimol, Ersland, & Hugdahl, 2004; Thomsen et al., 2004).

In the experimental design of the present study, first, the target sound was presented monaurally. Then, a dichotic pair including the probe sound was delivered. Within the dichotic pair, the probe sound was presented in the same ear that received the target sound and differed from it only by the intensity level. The other sound constituting the dichotic pair had a different spectral composition. The task of the subject was to judge whether target and probe sounds had different or equal intensity.

The working hypothesis of this study is related to a previous investigation on intensity coding of auditory stimuli (Jancke et al., 1998). That study reported that, during a binaural intensity discrimination task of verbal and non-verbal sounds, the voxel activation pattern in higher-order auditory cortex showed an asymmetry in favour of the right hemisphere. The present study aims at investigating whether this physiological asymmetry is related to a behavioural asymmetry. The prediction is that a left ear advantage indicative of a right hemisphere specialization should be found for sound intensity discrimination.