Elsevier

NeuroImage

Volume 103, December 2014, Pages 374-382
NeuroImage

Crossmodal plasticity in the fusiform gyrus of late blind individuals during voice recognition

https://doi.org/10.1016/j.neuroimage.2014.09.050Get rights and content

Highlights

  • Voice identity processing in late blind individuals was investigated using fMRI.

  • Late blind and matched sighted participants were tested in a S1-S2 paradigm.

  • Activation in the fusiform gyrus was modulated by voice identity in the blind only.

  • Similar crossmodal plasticity as in congenitally blind individuals was observed.

Abstract

Blind individuals are trained in identifying other people through voices. In congenitally blind adults the anterior fusiform gyrus has been shown to be active during voice recognition. Such crossmodal changes have been associated with a superiority of blind adults in voice perception. The key question of the present functional magnetic resonance imaging (fMRI) study was whether visual deprivation that occurs in adulthood is followed by similar adaptive changes of the voice identification system. Late blind individuals and matched sighted participants were tested in a priming paradigm, in which two voice stimuli were subsequently presented. The prime (S1) and the target (S2) were either from the same speaker (person-congruent voices) or from two different speakers (person-incongruent voices). Participants had to classify the S2 as either coming from an old or a young person. Only in late blind but not in matched sighted controls, the activation in the anterior fusiform gyrus was modulated by voice identity: late blind volunteers showed an increase of the BOLD signal in response to person-incongruent compared with person-congruent trials. These results suggest that the fusiform gyrus adapts to input of a new modality even in the mature brain and thus demonstrate an adult type of crossmodal plasticity.

Introduction

The efficient processing of socially relevant information such as the emotional state or the identity of another person forms the prerequisite for successful interactions between humans. Blind individuals rely almost exclusively on the auditory system to extract socially relevant information, i.e. they identify other people and infer their emotional states mainly through voices. Studies with congenitally blind individuals have revealed remarkable compensatory changes in various auditory functions (reviewed in Merabet and Pascual-Leone, 2010, Pavani and Röder, 2012) including voice processing. For example, congenitally blind people have been reported to show faster learning of voice identity (Föcker et al., 2012, Hölig et al., 2014), an enhanced memory for voices (Bull et al., 1983, Röder and Neville, 2003) and an improved discrimination of voice prosody (Klinge et al., 2010b). In addition, neuroplastic changes within the auditory cortex (intramodal plasticity), multisensory regions and the deafferented visual cortex (crossmodal plasticity, Merabet and Pascual-Leone, 2010, Pavani and Röder, 2012, Renier et al., 2014) have been demonstrated in a number of studies and are commonly discussed as underlying behavioral compensations in non-visual tasks including voice processing (Gougoux et al., 2009, Hölig et al., 2014). Recent reports have pointed out that the functional organization of visual cortical areas might be preserved after early visual deprivation (Renier et al., 2014, Voss and Zatorre, 2012) and visual areas respond to the functionally analogous non-visual input after vision loss. For instance, auditory spatial processing seems to recruit mainly dorsal areas (e.g. Collignon et al., 2011, Renier et al., 2010), while the processing of auditory or tactile object identity has been found to activate ventral areas of the visual cortex in congenitally blind individuals (Amedi et al., 2007, Amedi et al., 2010, Hölig et al., 2014, Pietrini et al., 2004).

Importantly, most findings on blindness-induced brain plasticity have been obtained from studies with congenital or early blind participants, i.e. from individuals who never had any visual experience or who lost vision early in life. Late blind adults have been less often investigated (Merabet and Pascual-Leone, 2010). In the present study we addressed the question of whether neural changes in the voice recognition system as they have recently been reported in congenitally blind individuals (Hölig et al., 2014) arise in individuals who had visual experience prior to blindness onset. Thus, we tested the question of whether or not crossmodal plasticity is linked to a sensitive phase in development.

Similar as in congenitally blind individuals, crossmodal plasticity in late blind individuals has been demonstrated for basic sensory functions, e.g. auditory localization (Voss et al., 2006, Voss et al., 2008) and pitch discrimination (Kujala et al., 1997), as well as for complex cognitive functions such as Braille reading (Büchel et al., 1998, Burton et al., 2002a) and language comprehension (Bedny et al., 2012, Burton and McLaren, 2006, Burton et al., 2002b, Burton et al., 2003).

Little research has been conducted on whether and how crossmodal plasticity differs between congenitally and late blind individuals. For example, a decrease in activation magnitude and distribution has been reported in late blind participants compared with congenital blind individuals in a series of studies by Burton et al. (Burton et al., 2002a, Burton et al., 2002b, Burton et al., 2003). Others have reported different activation foci within the occipital cortex for late blind and congenitally blind individuals (Büchel et al., 1998, Voss et al., 2008). Recent research has begun to identify qualitative differences. For instance, it has been shown that dorsal “visual” areas show a preference for the processing of sound motion (Bedny et al., 2010) and sound localization (Collignon et al., 2013) in congenitally blind but not in late blind individuals. Another study has reported that only congenitally blind but not late blind individuals show a left-lateralized activation for language processing in the occipital cortex (Bedny et al., 2012). Based on these findings, some researches tentatively proposed that the predetermined functional specialization of specific visual areas might be preserved in congenitally blind but not in late blind individuals (Bedny et al., 2010, Bedny et al., 2012, Collignon et al., 2013, Voss, 2013).

Whether blindness induced brain plasticity qualitatively differs between congenital and late blind individuals depends on the existence of critical periods for the development of functional specialized brain areas (Knudsen, 2004). Animal studies have shown that short periods of visual deprivation during early development have considerable consequences on the development of a number of visual cortical functions (Fagiolini et al., 1994, Hubel and Wiesel, 1970, Wiesel and Hubel, 1965). For example, monocular deprivation in the first months of life has been shown to permanently alter functional properties of V1 neurons and binocular vision in kittens (Hubel and Wiesel, 1970, Wiesel and Hubel, 1965). In humans, congenital cataracts cause enduring deficits in visual acuity (Lewis and Maurer, 2009) and in lip-reading capacities (Putzar et al., 2010). On the other hand, findings from studies on adult plasticity indicate that some neural systems remain plastic throughout life and are not constrained by early sensory experience (Bavelier and Neville, 2002, Gilbert and Li, 2012, Karmarkar and Dan, 2006).

It appears that some visual functions and underlying cortical circuits are permanently and irreversibly affected by early sensory experience whereas others maintain an enormous capacity for changes throughout life (Bavelier and Neville, 2002, Knudsen, 2004). The results of Collignon et al. (2013) and Bedny et al. (2010) suggest that spatial processing in the dorsal stream is particularly susceptible to the presence or absence of vision in early development. The sensory preference of this system seems to be enduringly shaped by the accessible modality during a time-constrained critical period. However, this does not exclude the possibility that other functional specialized systems of the deafferented visual cortex are malleable at all ages and alter their preferred sensory input according to environmental needs. This might be the case for the processing of object identity and object category in the ventral visual stream, as our capacity for the learning of new objects persists up to an old age and is constantly shaped by novel and sometimes unexpected environmental inputs (Bavelier and Neville, 2002; see Rao and Ballard, 1999 for a conceptual account). One particularly interesting example is the recognition of other individuals because we meet new people at all ages.

We have recently demonstrated that voice identity processing elicits activation in the right anterior fusiform gyrus in congenitally blind individuals but not in matched sighted participants (Hölig et al., 2014). On the other hand, voice identity priming was observed in the right posterior STS of sighted control but not of congenitally blind participants. Given that direct connections between voice-sensitive areas in the STS and face-sensitive areas in the fusiform gyrus exist (Blank et al., 2011), one might speculate that blindness may induce a “strengthening” or “expansion” of these connections which in turn leads to a reallocation of voice identity processing from the STS to the fusiform gyrus (Hölig et al., 2014). In the present study, we addressed the question of whether such neural changes in the voice recognition system following visual deprivation takes place in the mature brain. We first trained late blind and matched sighted participants to recognize unfamiliar voices in an extensive pre-experimental training and measured each participant’s voice recognition skills. Thereafter we employed a priming paradigm, in which we manipulated whether two successively presented voices belonged to the same speaker or to different speakers. As the fusiform gyrus has been found to respond to voice identity not only in the developing sensory deprived (Hölig et al., 2014) but also in the mature healthy brain (Von Kriegstein and Giraud, 2004, Von Kriegstein and Giraud, 2006, Von Kriegstein et al., 2005), we assumed that voice identity processing would elicit activation in the anterior fusiform gyrus of late blind individuals. We further hypothesized that if a reallocation of the voice identity system from the STS to the fusiform gyrus takes place in late blind participants, voice identity priming in the STS should be observed in sighted but not in late blind individuals.

Section snippets

Methods

The same methods of experimental design, data acquisition and data analysis as in Hölig et al. (2014) were applied.

Behavioral results

Late blind participants learned the voices within fewer training sessions than sighted participants (Table 1, t(14) = 2.38, p = 0.032), but did not differ from sighted participants in recognizing unknown pseudowords (Table 1, t(14) = 1.37, p = 0.192). On the day of scanning, voice recognition (Table 1, t(14) = 0.72, p = 0.484) and the performance in the voice matching task (Table 1, t(14) = 0.76, p = 0.459) did not differ between blind and sighted participants. Thus, blind and sighted participants showed

Discussion

The main question of the present study was whether changes in the voice identification occur in blindness of late onset as well. Behaviorally, late blind participants learned voices faster than sighted controls, i.e. sighted controls needed more training sessions to reach the same performance level as late blind participants. After the training, voice recognition skills did not differ between late blind and sighted participants. The processing of voices (auditory stimulation) elicited higher

Acknowledgments

We thank Katrin Wendt, Kathrin Müller and Corinna Klinge with their support acquiring the fMRI data and Jürgen Finsterbusch for setting up the fMRI sequence. We are grateful to Boris Schlaack for his support to create the stimulus material and to Ulrike Adam, Kirstin Grewenig and Florence Kroll for helping to record the stimulus material supervised by Prof. Dr. Eva Wilk. We thank the “Blinden-und Sehbehindertenverein Hamburg, e.V.”, the “Dialogue of the Dark” in Hamburg, and the “Tandem-Club

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