Activation lateralization in human core, belt, and parabelt auditory fields with unilateral deafness compared to normal hearing

Abstract

We studied activation magnitudes in core, belt, and parabelt auditory cortex in adults with normal hearing (NH) and unilateral hearing loss (UHL) using an interrupted, single-event design and monaural stimulation with random spectrographic sounds. NH patients had one ear blocked and received stimulation on the side matching the intact ear in UHL. The objective was to determine whether the side of deafness affected lateralization and magnitude of evoked blood oxygen level-dependent responses across different auditory cortical fields (ACFs). Regardless of ear of stimulation, NH showed larger contralateral responses in several ACFs. With right ear stimulation in UHL, ipsilateral responses were larger compared to NH in core and belt ACFs, indicating neuroplasticity in the right hemisphere. With left ear stimulation in UHL, only posterior core ACFs showed larger ipsilateral responses, suggesting that most ACFs in the left hemisphere had greater resilience against reduced crossed inputs from a deafferented right ear. Parabelt regions located posterolateral to core and belt auditory cortex showed reduced activation in UHL compared to NH irrespective of RE/LE stimulation and lateralization of inputs. Thus, the effect in UHL compared to NH differed by ACF and ear of deafness.

Introduction

Auditory cortex displays lateralization asymmetries despite binaural inputs. For example, the left hemisphere especially perceives and produces spoken language (Zatorre and Binder, 2000). Additionally, monaural stimulation normally evokes larger magnitude and shorter latency responses in the contralateral hemisphere (Jäncke et al., 2002, Khosla et al., 2003, Ponton et al., 2001, Vasama and Mäkelä, 1997, Zatorre and Binder, 2000). Each hemisphere also preferentially responds to different parameters of complex acoustic stimulation. Left auditory cortex generally is better at processing temporally complex, rapidly changing sounds characteristic of non-tonal speech; the right is more responsive to the tonal or spectral content of stimuli (Belin et al., 1998, Johnsrude et al., 2000, Obleser et al., 2008, Schönwiesner et al., 2005b, Scott et al., 2000, Scott et al., 2006, Tervaniemi and Hugdahl, 2003, Zatorre and Belin, 2001, Zatorre et al., 2002). Evidence of spectral representation in the left hemisphere (Obleser et al., 2008, Zatorre and Gandour, 2008) indicates that the temporal/spectral lateralization dichotomy is not especially rigid. Despite this caveat, unilateral sensorineural hearing loss (UHL) leads to behavioral deficits that may reflect lateralized processing of different sound parameters. Deficits with UHL include increased difficulty with understanding speech in noise (Bishop and Eby, 2010, Wie et al., 2010), and poorer sound localization (Abel et al., 1982, Humes et al., 1980).

Prior studies in patients with UHL reported changes in some aspects of auditory cortex asymmetry. In normal hearing, asymmetry involves greater contralateral hemisphere activation versus ipsilateral. In UHL, activation increased in the hemisphere ipsilateral to the intact ear with less change in the contralateral hemisphere leading to more balanced activation between hemispheres (Bilecen et al., 2000, Langers et al., 2005, Ponton et al., 2001, Scheffler et al., 1998). These lateralization changes in UHL were attributed to primary auditory cortex based on identifying Heschl's gyrus as the site of activity (Bilecen et al., 2000, Langers et al., 2005, Scheffler et al., 1998, Tschopp et al., 2000).

Few studies examined the effect of ear of deafness on cortical lateralization patterns. Right ear (RE) stimulation evoked equivalent ipsilateral and contralateral activation and left ear (LE) stimulation yielded larger contralateral responses (Hanss et al., 2009, Khosla et al., 2003, Schmithorst et al., 2005). An objective of the current study was to examine hemispheric asymmetries with respect to stimulated ear in different auditory cortex fields (ACFs).

Initial descriptions of ACFs arose from neurophysiological assessments of tonotopic organization in macaques and other animals. These findings included tonotopic mapping with pure tones in core (primary auditory, A1, rostral area, R, and rostral–temporal area, RT), surrounding belt (rostro-middle, RM, rostro-temporal-middle, RTM, caudo-medial, CM, caudo-lateral, CL, middle-lateral, ML, antero-lateral, AL and rostro-temporal–lateral, RTL), and lateral parabelt auditory fields (caudal parabelt, CPB and rostral parabelt, RPB) (Imig et al., 1977, Kaas and Hackett, 2000, Merzenich and Brugge, 1973).

Tonotopic maps obtained in fMRI studies in humans have noted mirror reversals across successive ACFs in core and belt regions (da Costa et al., 2011, Humphries et al., 2010, Striem-Amit et al., 2011, Woods et al., 2009, Woods et al., 2010). Core regions with sharply defined tonotopic organization occupy much, but not all of Heschl's gyrus (da Costa et al., 2011, Penhune et al., 1996, Rademacher et al., 1993). As in animals, the core region of auditory cortex has a koniocortex cytoarchitecture and the surrounding cortex shows decreased layer IV thickness (Brodmann, 1909, Galaburda and Sanides, 1980, Morosan et al., 2001, Rademacher et al., 2001, von Economo, 1929). Based on quantitative and objectively defined criteria, these cytoarchitectonic differences along the superior temporal plane and gyrus show five subdivisions: Te1.0, Te1.1, Te1.2, Te2 and Te3 (Morosan et al., 2001, Rademacher et al., 2001).

Woods and colleagues overlaid acoustically activated regions onto average gyral and sulcal landmarks to relate different ACFs to the Te subdivisions (Downer et al., 2011, Woods and Alain, 2009, Woods et al., 2009). They showed that Te1.1 encompasses caudomedial A1 core and part of medial belt areas (RM, CM); Te1.0 centers on core AFCs (medial A1 and caudal R); Te1.2 also includes some core ACFs (R rostrally and RT caudally); and Te3 comprises lateral belt ACFs (AL and ML). Additionally, based on myelin boundaries (Glasser and Van Essen, 2011), Te2 partially embraces caudal parts of core A1 and caudal belt ACFs (CL); and STG/STS-BA22 contains lateral belt (CL) and parabelt ACFs (CPB). A major objective of the current study was to contrast results from each of the Te defined regions and their associated ACFs from two hearing groups, UHL and normal hearing (NH).

Most prior studies in UHL used simple stimuli such as pure tones (Schmithorst et al., 2005), 1000 Hz pulsed tones or tone bursts (Bilecen et al., 2000, Hanss et al., 2009, Scheffler et al., 1998, Tschopp et al., 2000, Vasama and Mäkelä, 1997), click trains (Khosla et al., 2003, Ponton et al., 2001), and narrowband noise (Langers et al., 2005, Propst et al., 2010). A few used speech in quiet (Firszt et al., 2006, Hanss et al., 2009) or in noise (Propst et al., 2010). While simple stimuli avoid possible confounds due to the linguistic content of speech, simple stimuli generally suffer from bandwidth-by-duration limitations. All the random spectrogram sound (RSS) stimuli employed in the current study have, on average, the same spectral bandwidth and duration, and hence do not suffer from this bandwidth-by-duration limitation. Furthermore, all RSS stimuli had, on average, matching intensities across the same spectral region for the same time period, thereby removing intensity or spectral bandwidth or duration as potential confounding variables. In addition, RSS stimuli allowed for independent control of spectral complexity (akin to bandwidth) and temporal complexity (akin to duration) (Schönwiesner et al., 2005b). The RSS probed response differences associated with sounds distinct from speech, music, or pure tones. The current study therefore assessed the temporal/spectral dichotomy hypothesis by comparing auditory cortex activation distributions to monaural RSS (Schönwiesner et al., 2005b) in adults with left or right unilateral deafness and in similar age adults with normal hearing. A sparse sampling, single-event BOLD design (Amaro and Barker, 2006, Belin et al., 1999) also allowed examination of response time courses to the stimuli.