A brain of two halves: Insights into interhemispheric organization provided by near-infrared spectroscopy

NeuroImage 85 (2014) 354–362

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Review

A brain of two halves: Insights into interhemispheric organization provided by near-infrared spectroscopy Fumitaka Homae ⁎ Department of Language Sciences, Tokyo Metropolitan University, 1-1 Minami Osawa, Hachioji, Tokyo 192-0397, Japan

a r t i c l e

i n f o

Article history: Accepted 3 June 2013 Available online 14 June 2013 Keywords: Cognitive neuroscience Corpus callosum Development Infant Inhibition Laterality

a b s t r a c t The discovery of functional lateralization and localization of the brain marked the beginning of a new era in neuroscience. While the past 150 years of research have provided a great deal of knowledge of hemispheric differences and functional relationships, the precise organization of functional laterality remains a topic of intense debate. Here I will shed light on the functional organization of the two hemispheres by reviewing some of the most recent functional near-infrared spectroscopy (NIRS) studies that have reported hemispheric differences in activation patterns. Most NIRS studies using visual stimuli, which revealed functional differentiation between the hemispheres, have reported unilateral activation, i.e., significant levels of activation in only one hemisphere. Auditory stimuli, including speech sounds, elicited bilateral activation, while the limited number of studies on young infants revealed primarily unilateral activation. The stimulus modality and the age of the participants therefore determine whether the resulting cortical activation is unilateral or bilateral. By combining a review of the existing literature with NIRS results regarding homologous connectivity across hemispheres, I hypothesized that the origin of functional lateralization changes from the independence of each hemispheric region, to mutual inhibition between homologous regions during development. Future studies applying multi-modal measurements along with NIRS and spatiotemporal analyses will further deepen our understanding of the interhemispheric organization of brain function. © 2013 Elsevier Inc. All rights reserved.

Contents Introduction . . . . . . . . . . . . . . . . . . . . . . Hemispheric differences in brain structure . . . . . . . . Hemispheric differences in brain function . . . . . . . . The role of the corpus callosum in functional differentiation The development of interhemispheric connectivity . . . . Lateralization and unilateral activation in the brain revealed Future directions . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . . Conflict of interest . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . by NIRS . . . . . . . . . . . . . . . . . . . .

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Introduction The human cerebrum consists of two hemispheres: the left and right hemispheres. In adults, the two hemispheres are not mirror images, but show numerous macroscopic anatomical asymmetries ⁎ Fax: +81 42 677 2160. E-mail address: [email protected]. 1053-8119/$ – see front matter © 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.neuroimage.2013.06.023

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(Toga and Thompson, 2003). The right frontal lobe protrudes anteriorly, and is wider than the left frontal lobe, with the occipital lobe showing the opposite trend. As a result, the volumes of the frontal and occipital regions differ between the hemispheres; the right frontal lobe is larger than the left, and the left occipital lobe is larger than the right. Other anatomical asymmetries include the gentler curve of the left Sylvian fissure (Hochberg and Le May, 1975; Sowell et al., 2002), and the wider area of the left planum

F. Homae / NeuroImage 85 (2014) 354–362

temporale (Geschwind and Levitsky, 1968; Good et al., 2002). Besides such morphological differences, the left and the right hemispheres show marked functional differences, i.e., brain functions are lateralized. The functional difference between the two hemispheres was first reported in the domain of language functions, where it was demonstrated that the left hemisphere is dominant in language processing (Damasio and Geschwind, 1984). Our understanding of hemispheric differences and interhemispheric communication was considerably deepened through a series of studies on split-brain patients (for a review, see Gazzaniga, 2000). In addition to the surgical disconnection of the cerebral hemispheres, clinical studies on agenesis of the corpus callosum (AgCC) have improved our understanding of hemispheric interactions (Friederici et al., 2007; Paul et al., 2007). The development of functional neuroimaging methods, such as positron emission tomography (PET) and functional magnetic resonance imaging (fMRI), further facilitated the characterization of the laterality of multiple brain functions. Thus, the different roles of the two hemispheres, and their cooperative function, have long been a fundamental topic in cognitive neuroscience. In this review, I will focus on the functional organization of the two hemispheres by examining some of the recent functional near-infrared spectroscopy (NIRS) studies that have reported hemispheric differences in neural activation patterns. Because NIRS methodology makes it feasible to record brain activation in infants, many of these studies have compared activation in the left and right hemispheres of infants, and differences between infants and adults. Thus, my main discussion will concentrate on developmental aspects of cerebral laterality. I will combine this review of the literature with our NIRS results on homologous connectivity across the hemispheres, to develop a hypothesis regarding the functional development of the interhemispheric organization of the brain. The importance of NIRS measurements in cognitive neuroscience is demonstrated through the consideration of cerebral specialization and interaction. There have been a number of excellent reviews on the use of NIRS in cognitive neuroscience (Aslin, 2012; Dieler et al., 2012; Gervain et al., 2011; Lloyd-Fox et al., 2010; Minagawa-Kawai et al., 2008; Obrig et al., 2010; Quaresima et al., 2012; Rossi et al., 2012), most of which focused on stimulus-driven activation of the cortex. The present review attempts to merge our knowledge of brain structure with spontaneous and functional activation data obtained by NIRS studies, in order to examine the background neural systems underlying cognitive functions. Hemispheric differences in brain structure The recent accumulation of structural evidence from MRI studies has begun to clarify how the brain develops throughout infancy and childhood (Almli et al., 2007; Evans, 2006). One MRI study reported that the left hemisphere of neonates in the first few weeks after birth was larger than the right hemisphere, and that the frontooccipital asymmetry commonly observed in adults was not present (Gilmore et al., 2007). This study also demonstrated that the gray matter of the occipital and parietal regions grew significantly faster than that of the prefrontal region. In contrast, during the first 2 years after birth, the frontal lobes grew more rapidly than the temporal lobes, and that the right frontal and temporal lobes showed a greater increase in volume than the left frontal and temporal lobes (Matsuzawa et al., 2001). Recently, Tanaka et al. (2012) reported the developmental trajectories of the frontal and temporal lobes from 1 month to 25 years old. The volumetric changes were non-linear in all regions, and gray matter volume reached its peak at an earlier age in the frontal lobe than in other regions. Moreover, the left frontal and temporal lobes continued to increase in volume for a longer period of time than the same regions in the right hemisphere. These studies suggest that development of the cerebral cortex is not straightforward, and that the speed of maturation in

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the frontal region is selectively accelerated after the neonatal period. The cerebral blood flow pattern at rest also showed hemispheric differences in infancy and early childhood. Although no hemispheric difference could be detected before 1 year of age, there was a right hemispheric dominance between 1 and 3 years of age, and asymmetrical shifts to the left hemisphere after 3 years of age (Chiron et al., 1997). This study suggests that both structural asymmetry and functional asymmetry occur prior to 3 years of age. Hemispheric differences in brain function Behavioral studies have suggested that the left and right hemispheres of infants younger than 1 year work differentially (Bertoncini et al., 1989; Holowka and Petitto, 2002). High-density recordings of event-related potentials (ERPs) have also demonstrated the asymmetrical distribution of evoked potentials over the scalp while the subject is hearing phonological or syllabic stimuli (Dehaene-Lambertz, 1997; DehaeneLambertz and Dehaene, 1994). More recently, speech perception and face processing have been examined using neuroimaging methods such as fMRI and PET, and the neural activation patterns evoked by speech and face stimuli were reported to be consistent between infants and adults (Dehaene-Lambertz et al., 2002; Tzourio-Mazoyer et al., 2002). Recent NIRS studies and reviews have compared the laterality characteristics of infants with those of adults. One interesting topic is the relative sensitivity of the left and right hemispheres to the temporal structure of sounds (Minagawa-Kawai et al., 2011a; Telkemeyer et al., 2009, 2011). The sensitivity of the two hemispheres in adults has been extensively debated, and several possible mechanisms have been proposed to explain the relationship to language processing (McGettigan and Scott, 2012; Poeppel et al., 2008; Tervaniemi and Hugdahl, 2003; Zatorre and Gandour, 2008; Zatorre et al., 2002). Telkemeyer et al. (2009, 2011) showed that neural responses to slow acoustic modulations are lateralized in the right hemisphere of neonates, 3-month-old infants, and 6-month-old infants. This trend of right hemisphere lateralization is consistent with the findings of a previous fMRI study in adults (Boemio et al., 2005). However, Minagawa-Kawai et al. (2011a) reported bilateral activation if neonates, in response to both rapidly and slowly modulated sounds. The authors of the previous study state that “our results line up with the previous newborn study, where the evidence for lateralization was scarce (one-tailed t-test on 1 channel selected among 6, 0.03 b puncorr b 0.05; Telkemeyer et al., 2009)” (p. 9), and they hypothesized that functional asymmetries might develop during early infancy. Although the conclusions of the two studies are not consistent, both are important not only in the context of understanding the acoustic and speech-sound processing of infants, but also in the context of examining the relationship between the two cerebral hemispheres. If the left and right temporal regions develop to utilize different mechanisms, or perhaps different time scales of acoustic processing during early development, the question remains of how these functionally differentiated regions interact with each other. The formation of the brain structure, which connects these homologous regions, namely the corpus callosum, plays a key role in these interactions. The role of the corpus callosum in functional differentiation The left and right hemispheres of the human brain are connected by three major commissural fibers: the anterior commissure, the hippocampal (or posterior) commissure, and the corpus callosum, the last of which is the largest (composed of more than 200 million fibers), and exists only in placental mammals. The corpus callosum has a topographical distribution of fiber connections, and can be divided into morphologically distinct subregions, which correspond to the cortical regions that the fibers connect. The fiber size and

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F. Homae / NeuroImage 85 (2014) 354–362

Fig. 1. Homologous connectivity in neonates, 3-month-old infants, and 6-month-old infants. The spontaneous activation of the infant brain reported in our previous study (Homae et al., 2010) was reanalyzed. (A) Depiction of the virtual registrations of measurement channels, and the boundaries of the frontal, temporal, parietal, and occipital lobes. Axes correspond to those in MNI space (see, Watanabe et al., 2013). Yellow circles indicate the positions of the measurement channels, and orange circles indicate the locations of 10–20 cortical projection points on the brain surface. We placed 47 measurement channels over each hemisphere. The black lines indicate borderlines between lobes based on Watanabe et al. (2013). (B) 94 measurement channels and 47 homologous pairs. The borderlines of the four lobes shown in (A) were superimposed on the left hemisphere. (C–E) Homologous connectivity in each measurement channel. The participant groups were neonates (C), 3-month-old infants (D), and 6-month-old infants (E). Red, magenta, yellow, green, and cyan filled circles indicate measurement channels that showed averaged correlations higher than 0.7, 0.6, 0.5, 0.4, and 0.3, respectively. Note that the frontal regions in neonates showed high correlations between homologous channels. In general, the level of correlation in the temporal, parietal, and occipital regions increases with the age of the infants. The temporal regions of the 3-month-old infants show lower correlations in compared to the parietal regions.

Fig. 2. Mean homologous connectivity of each lobe. I calculated the temporal correlation between all the pairs of homologous channels (47 pairs), and averaged the obtained correlation coefficient (r) among the channels in each lobe. Blue, red, and green bars indicate the mean value of each lobe among the participant group of neonates, 3-month-old infants, and 6-month-old infants, respectively. The error bars represent standard deviations among the participants. The asterisks indicate the level of significance in the post hoc analyses after performing Fisher's z-transformation (*p b 0.05, **p b 0.005, and ***p b 0.0005).

density within the corpus callosum varies according to the subregions. Thick fibers connect the primary sensory regions, and thinner fibers connect association regions. One of the thickest fibers is the callosal fiber, which connects the primary and secondary auditory areas (Aboitiz et al., 1992). The myelination of these fibers continues through puberty, and the degree of myelination depends on the individual. Interindividual variation in the size of the corpus callosum was found to be negatively correlated with behavioral laterality in dichotic listening tasks (Yazgan et al., 1995). This study suggested two important points: 1) the composition of the corpus callosum can affect behavior, and 2) the corpus callosum assumes a facilitative role when the participant was performing tasks. If the corpus callosum transfers a large amount of information from one hemisphere to the other, it follows that each hemisphere receives auditory information presented to both ears. It would be more difficult to select a single auditory information in this situation, resulting in worse performance on the dichotic listening task. There are at least two different perspectives on the relationship between callosal connectivity and the lateralization of function (Bloom and Hynd, 2005; Raybaud, 2010; van der Knaap and van der Ham, 2011). The excitatory model proposes that the corpus callosum conveys information from one hemisphere to the other, shares the information between the hemispheres, and stimulates the other hemisphere. The dichotic listening studies such as that described above support this view. In contrast, the inhibitory model posits that the corpus callosum does not excite the other hemisphere, and maintains independent processing between the hemispheres. Interhemispheric inhibition has been observed in the visual, motor,

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357

Table 1 Previous NIRS studies reporting hemispheric differences in activation. Visual stimuli Author(s)

Year

Age

Experimental condition vs baseline condition

Region

Lateralization

L

R

U

v1

Grossmann et al.

2008

4

F, T

R>L

×

○

○

v2

Grossmann and Johnson

2010

5

F

L>R

○

×

○

v3

Lloyd-Fox et al.

2011

5

T

R>L

×

○

○

v4

Otsuka et al.

2007

5 to 8

T

R>L

×

○

○

v5

Nakato et al.

2009

5

Mutual gaze Moving cars Joint attention Non-social moving stimuli Mouth movement Mechanical condition Upright face Inverted face Frontal face Profile face Profile face Frontal face Number-/shape-deviant Adaptation image Audiovisual stimuli Visual stimuli Facial biological motion Still frames Action observation Object-motion observation Smile own-infant face Neutral own-infant face

T

R>L

×

×

-

T

R>L

×

○

○

P, O

R>L

×

○

○

T

L>R

○

×

○

T

R>L

×

○

○

F

L>R

○

×

○

F

R>L

×

○

○

8 v6

Hyde et al.

2010

6

v7

Bortfeld et al. (a)

2009

6 to 9

v8

Ichikawa et al.

2010

7 to 8

v9

Shimada and Hiraki

2006

Adult

v10

Minagawa-Kawai et al.

2009

Adult

Auditory stimuli Author(s)

Year

Age

Experimental condition vs baseline condition

Region

Lateralization

L

R

U

a1

Peña et al.

2003

0

T

L>R

○

×

○

a2

Gervain et al.

2008

0

F, T

L>R

○

○

–

a3

Telkemeyer et al.

2009

0

TP

R>L

×

×

–

a4

Kotilahti et al.

2010

0

T

L>R

○

○

–

a5

Arimitsu et al.

2011

0

a6

Gervain et al.

2012

0

T P F, T

R>L L>R L>R

○ ○ ○

○ × ○

– ○ –

a7

Sato et al.

2012

0

TP

L>R

○

×

○

a8

Homae et al.

2006

3

TP

R>L

○

○

–

a9

Telkemeyer et al.

2011

3

Forward speech Backward speech/silence Syllable sequences (ABB) Syllable sequences (ABC) Slow modulated stimuli Fast modulated stimuli Forward speech Silent Phonemic/prosodic contrasts Identical word presentation Syllable sequences (AAB) Syllable sequences (ABC) Forward speech Backward speech Normal/flattened speech Silent Fast/slow modulated stimuli Silent Fast/slow modulated stimuli Silent

F T T TP F TP TP

L>R L>R L>R R>L R>L R>L R>L

×

×

–

×

×

–

○

○

–

T

L>R

○

×

○

T

R>L

×

○

○

TP

R>L

○

○

–

T

L>R

○

○

–

T

L>R

○

○

–

T

L>R

○

○

–

F, T T T

× × ○

× × ○

– – –

○

○

–

○

○

–

T

L>R R>L L>R R>L L>R R>L L>R R>L L>R

○

○

–

T

L>R

○

○

–

6

a10

Homae et al.

2012

3, 6

a11

Minagawa-Kawai et al.

2011b

4

a12

Grossmann et al.

2010

7

a13

Homae et al.

2007

10

a14

Sato et al.

2010

10

a15

Minagawa-Kawai et al.

2007

13 to 14 25 to 28

a16

Wartenburger et al.

2007

4y

a17

Sato et al.

2011

3–5 y 6–10 y Adult

a18

Sato et al.

1999

Adult

a19

Minagawa-Kawai et al.

2002

Adult

3 types of tone sequences Silent Native/non-native speech Silent Emotional prosody Silent Normal/flattened speech Silent Pitch contrast (words) Identical word presentation Vowel contrast Identical word presentation Vowel contrast Identical word presentation Normal/hummed/flat speech Silent Phonemic/prosodic contrasts Identical word presentation Phonemic/prosodic contrasts Identical word presentation Phonemic/prosodic contrasts Identical word presentation Story/repeated sentences Pure tone with white noise Vowel contrast Identical word presentation

T T

*1 *1 *2 *2 *3 *3

*4 *5 *6 *7 *6 *7 *6 *7

(continued on next page)

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Table 1 (continued) Visual stimuli Auditory stimuli Author(s)

Year

Age

Experimental condition vs baseline condition

Region

Lateralization

L

R

U

a20

Sato et al.

2007

Adult

TP

L>R

○

○

–

a21

Hull et al. (b)

2009

Adult

T

L>R

○

×

○

a22

Rossi et al.

2011

Adult

Accent/phoneme/word contrasts Identical stimuli Picture naming Silent Legal pseudowords Illegal pseudowords

T

L>R

○

×

○

Previous NIRS studies reporting hemispheric differences are summarized here. The y in the age column indicates years. Otherwise, the numbers in the age column indicate months. F, T, P, and O in the region column indicate the frontal, temporal, parietal, and occipital lobes, respectively. TP indicates the temporoparietal region. Lateralization shows the dominant hemisphere, which the previous study reported (L: left hemisphere, R: right hemisphere). In the L and R columns, the study that reported significant activity either in the left or right hemisphere is marked “○.” The “×” marks indicate that the study did not report any significant activity in the experimental condition compared with the baseline condition. The marks of “o” in the U (unilaterality) column indicate that significant activity was reported only in one hemisphere. (a) Bortfeld et al. (2009) used audiovisual stimuli. (b) Hull et al. (2009) used a production task. *1 fast or slow modulated sounds, *2 fast modulated sounds, *3 slow modulated sounds in Telkemeyer et al. (2011), *4 normal speech, *5 hummed stimuli and flat stimuli in Wartenburger et al. (2007). *6 phonemic contrast, *7 prosodic contrast in Sato et al. (2011).

and somatosensory cortices (Ferbert et al., 1992; Innocenti, 2009; Jung et al., 2012). A negative correlation between the size of callosal fibers and performance on a motor task has also been recently reported (Kurth et al., in press). This inhibition of homologous activation would act to facilitate functional asymmetry and the lateralization of the brain during development. The correlation between callosal fiber sizes and behavioral performance depended on the specific tasks performed (Clarke and Zaidel, 1994), suggesting that an excitatory or inhibitory role is not always dominant. Although many studies support the excitatory model, excitation and inhibition may occur simultaneously, and their order of priority might depend upon the developmental stages of the brain, and the specific processing that the brain undergoes. Hereafter, I will mainly focus on the functional relationships between homologous regions, and functional lateralization during the early stages of development. First, I will investigate developmental changes in homologous connectivity by reanalyzing our NIRS data recording spontaneous activity obtained from neonates, 3-month-old infants, and 6-month-old infants (data from Homae et al., 2010). These results will be discussed in relation to our anatomical knowledge of the growth of the corpus callosum in early infancy (Section The development of interhemispheric connectivity). Second, the hemispheric differences in activation patterns reported across multiple NIRS studies will be reviewed. While many studies revealed activation in both hemispheres, others showed activation only in one hemisphere. These bilateral and unilateral activation patterns can potentially be explained by several possible factors. Finally, I will summarize the results of studies on homologous connectivity and unilateral activation and propose a hypothesis regarding interhemispheric relationships in the developing brain (Section Lateralization and unilateral activation in the brain revealed by NIRS). The development of interhemispheric connectivity Multi-channel NIRS is an effective and practical method to measure cortical activation in infants. Our research group has recorded the frontal, temporal, parietal, and occipital lobe activation patterns of infants by using 94-channel NIRS (Homae et al., 2011; Taga et al., 2011; Watanabe et al., 2013). The advantage of multichannel measurements covering broad cortical regions lies not only in determining functional localizations, but also in allowing the examination of functional relationships between multiple cortical regions simultaneously. Our previous study, which focused on the development of functional connectivity in early infancy, reported that homologous regions in the temporal, parietal, and occipital regions showed increases in their strength of connectivity from 3 to 6 months of age (Homae et al., 2010). Here, I reanalyzed the recordings of 3-min epochs of spontaneous activity obtained from neonates (N = 16), 3-month-old infants (N = 21), and 6-month-old infants

(N = 15) in order to more precisely reveal the spatial distribution of the developmental changes. The 94 measurement channels were arranged symmetrically on the infants' heads, and comprised 47 pairs of homologous channels. For each infant, the temporal correlation of 3-min data (oxyhemoglobin signals; sampling rate, 10 Hz; 1800 time points) between homologous channels was calculated. Following this individual analysis, I determined the group average for each channel pair. Fig. 1 shows the averaged correlation coefficients between infants for each homologous pair of brain regions. According to the virtual registration of measurement channels on brain surface reported in our previous paper (Watanabe et al., 2013), the 47 measurement channels on each hemisphere were parceled out into four lobes, namely, the frontal, temporal, parietal, and occipital lobes (Figs. 1A and B). The neonatal group showed correlation coefficients higher than 0.5 only in the frontal lobe (Fig. 1C). The channels in the temporal, parietal, and occipital lobes scored lower coefficients. The correlations in the 3-month-old group were higher than those in the neonatal group in general (Fig. 1D). Overall, homologous correlation showed high values, as was the case in our previous study with adult participants (Sasai et al., 2011). Most of the channels on the parietal and occipital lobes showed correlations higher than 0.6, while the values for channels on the temporal lobes were between 0.5 and 0.6, which were lower than those of the parietal and occipital channels. This trend was also observed in the 6-month-old group (Fig. 1E); the majority of the channels on the parietal and occipital lobes showed correlations higher than 0.7, while the values of the channels on the temporal lobes were between 0.5 and 0.7. Although the correlations between homologous regions were rather high in the 3- and 6-month-old groups, the progress of developmental changes was dependent on the specific cortical region. I calculated the mean correlation values for each lobe (Fig. 2), and applied an analysis of variance (ANOVA) with two factors (three infant groups and four lobes) after performing Fisher's z-transformation. I found significant main effects of the infant group (F(2,49) = 7.726, p b 0.005) and the lobe (F(3,147) = 15.348, p b 0.001). Post hoc analysis (Ryan's method) revealed that the mean correlations in neonates were lower than those in either 3-month-old infants (p b 0.05) or 6-month-old infants (p b 0.001). The interaction between infant group and lobe was also significant (F(6,147) = 6.461, p b 0.001). In neonates, the frontal lobe showed a higher correlation than the other three lobes (see asterisks in Fig. 2). A significant difference between the frontal lobe and the temporal lobe was also observed in the 3-month-old infants, suggesting that the development of homologous connectivity in the temporal lobe is relatively slower than that in other lobes. In contrast, the 6-month-old infants did not show any such differences. While the correlations in the temporal, parietal, and occipital lobes increased with the age of the infants, the frontal lobe did not display any age-dependent differences in correlations. These analyses supported the

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above observations. The positive values of the correlation coefficients suggest that homologous regions were synchronized in phase, and that the connectivity between these regions was excitatory when no stimulus was presented. The development of the frontal regions proceeds first from the neonatal period, and probably from the fetal period, with development of parietal and occipital connectivity following that of the frontal regions. The homologous correlations in the temporal region, particularly in the inferior temporal region, increase in strength relatively slowly (Fig. 1). The order of this development, proceeding from the frontal to the parietal and temporal regions, is the same as the arrangement of the subregions in the corpus callosum (Berlucchi, 2012); the fibers connecting the left and right inferior temporal regions are located posterior and inferior to the fibers connecting the parietal regions (Hofer and Frahm, 2006). These results are consistent with the findings from a study by Rakic and Yakovlev (1968), in which the researchers demonstrated that the corpus callosum develops from front to back; the frontal segment of the corpus callosum develops prenatally, and the splenium develops primarily postnatally. The myelination of callosal fibers is thought to proceed from posterior regions (the isthmus and splenium) to anterior regions (the body, genu, and the rostrum) (Raybaud, 2010), so increases in the functional connectivity in the occipital regions would occur earlier than in the temporal regions, including the temporal association areas. This developmental pattern of homologous connectivity would be expected to affect the functional organization of the cortex, and in particular its functional lateralization. Lateralization and unilateral activation in the brain revealed by NIRS The hemispheric dominances of perceptual and cognitive functions have been examined using both fMRI and NIRS. Most of the studies using NIRS addressed the subject of lateralization in the infant brain. I have surveyed the previous NIRS studies that have reported hemispheric differences in cortical activation, and divided the studies into two groups on the basis of the stimulus modality: auditory or visual (Table 1). The majority of studies tested infants younger than 10 months old, children ranging from 3 to 10 years old, or adults, using various experimental/baseline conditions and statistical thresholds. I examined whether these studies reported significant activation in homologous regions of the cortex, or in a single hemisphere. Interestingly, a clear difference arises between stimulus modalities. All 10 studies using visual stimuli demonstrated not only a hemispheric difference of signal changes between the left and the right hemispheres, but also unilaterality, i.e., significant activation was reported only in one hemisphere, in the association areas. Six (v1, v3, v4, v5, v7, and v8) and 4 (v1, v2, v9, and v10) out of 10 studies showed unilateral activity in the temporal and frontal regions, respectively. The results of the auditory stimuli studies offer a contrast to those using visual stimuli. Only 7 (a1, a5, a6, a11, a12, a21, and a22) out of 22 studies using auditory stimuli found unilateral activity. Six (a1, a5, a11, a12, a21, and a22) of these revealed unilateral activity in the temporal regions. This difference between the visual and auditory modalities is likely a reflection of modality-dependent processing in the cerebral cortex. The left and right temporal regions are considered to play distinct roles during auditory processing. While the temporal region in one hemisphere is activated in response to a feature of auditory stimulation, such as changes in the short temporal window (Poeppel et al., 2008), the corresponding temporal region in the other hemisphere could be responsive to other features of the stimulus, such as changes in the long temporal window (Poeppel et al., 2008), resulting in bilateral activation. The information processed in each hemisphere will be integrated after the distinct processes have been performed, if the corpus callosum assumes the excitatory role. Consequently, it is almost impossible to demonstrate unilateral

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activation in the temporal regions when auditory stimuli are presented. In contrast, the temporal regions showed unilateral activation in response to visual stimuli. Thus, interhemispheric transfer via the corpus callosum is dependent on the input modality. A crossmodal comparison of activations in bilateral regions around the superior temporal sulcus, which is considered to be a multimodal region, will shed light on this modality dependency. There are two other possibilities that could account for the differences between the visual and auditory studies. One is the difference in baseline conditions between visual and auditory studies. If a baseline condition activated only one hemisphere, the contrast between an experimental condition and the baseline condition would be likely to induce unilateral activation. Moreover, if a baseline condition was far from the experimental condition, both hemispheres would show differential activation in the contrast, resulting in bilateral activation. Although unilateral activation was observed in the auditory studies irrespective of their baseline conditions (either silent or non-silent conditions), the selection of both experimental and baseline conditions should be carefully considered when laterality and unilaterality are concerned. The other possibility is the sleeping or awake status of infants when they are assessed; the infants who participated in the studies using visual stimuli were, by necessity, awake, while some of the infants in the auditory stimulation studies were asleep. However, since 2 neonate studies conducted while the infants were sleeping (Arimitsu et al., 2011; Peña et al., 2003) reported unilateral activity in the left temporal or parietal region, the waking state of infants cannot fully explain these differences observed. Nevertheless, activated regions in infants in the sleeping state were often wider than in those who were awake (Homae et al., 2012; Taga and Asakawa, 2007). Sleep might either facilitate the excitation, or reduce the inhibition between cortical regions, both of which are likely to induce bilateral activation. Table 2 summarizes the interhemispheric connectivity shown in Figs. 1 and 2, and the unilateral activation in Table 1. As shown in this table, the temporal and parietal regions in neonates showed lower homologous connectivity, and unilateral activity (Arimitsu et al., 2011; Peña et al., 2003; Sato et al., 2012). The independence of bilateral regions reflects the lower connectivity between homologous regions, leading to the unilaterality of functional activations in the neonate brain. On the other hand, all regions except for the inferior temporal regions of 6-month-old infants showed higher homologous connectivity, and unilateral activity. If the homologous connections always assume the excitatory role, bilateral activation would be observed in both visual and auditory studies in infants of or around this age. Taking the unilateral activity in the association areas into consideration, homologous regions at this age would have inhibitory connections when the cortical regions are activated by visual or auditory stimuli. In other words, the origin of unilateral activity changes with age, from lesser connectivity between, or independence of homologous regions (in neonates), to the inhibition of homologous activation (in 6-month-old infants) during early development. The intrahemispheric connections also mature in this period, resulting in an expansion of the white matter. If the cortico-cortical connections between adjacent regions have inhibitory functions (e.g., inhibitory interneurons), the unilateral activity observed in relatively older infants and adults is predicted to be the result of both interhemispheric and intrahemispheric inhibition of cortical activation. NIRS studies can address the issues of interhemispheric transfer and functional asymmetry of the brain, by investigating the localization of neural activity across a broad age range of participants, including neonates and infants. Future directions My hypothesis should be verified by future studies. Mapping the homologous relationships in infants more than 6 months old needs to be performed by measuring spontaneous activations of the brain.

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Table 2 Hemispheric connectivity and unilateral activation. Frontal

Temporal

Parietal

Occipital

Months

HC

A

V

HC

A

V

HC

A

V

HC

A

V

0 3 6

H H H

× × ×

– ○ ○

L M H

○ ○ ○

– ○ ○

L H H

○ × ×

– – ○

L H H

– × ×

– – ○

Homologous connectivity in neonates (0), 3-month-old infants (3), and 6-month-old infants (6) are arranged with the existence (○) or absence (×) of NIRS studies that reported unilateral activation. HC: homologous connectivity, H: high correlation (correlation coefficient, r > 0.6), M: middle correlation (0.6 > r > 0.4), L: low correlation (r b 0.4), A: studies using auditory stimuli, V: studies using visual stimuli, –: no reports.

The functional activation data obtained thus far from infants aged from 10 months to 4 years are not sufficient to definitively support any single hypothesis. Furthermore, most of NIRS studies cited in this review (with the exception of Homae et al., 2012 and Sato et al., 2012) measured cortical activation in limited areas and involved positioning of the measurement channels over the temporal regions when auditory stimuli were presented. The NIRS recordings and correlation analyses of broader cortical regions would provide critical information for improving the hypothesis. With regard to neonates, their lower functional connectivity between homologous regions may be a reflection of relative independence, both in the spontaneous fluctuations and functional activation, although their correlation coefficients had positive values. NIRS data from preterm infants and neonates help to reveal the excitatory and inhibitory roles of the corpus callosum during the neonatal period. The collection of such NIRS data, as well as building a consensus regarding data-analysis procedures, and the subsequent refinement of our explanations would be useful to reveal details of the functional development of the brain from infancy, childhood, adolescence, and into adulthood. In order to understand the relationships between the homologous cortical regions, the difference in the timing of activation between the hemispheres might provide an important clue. One candidate method for achieving this objective is the analysis of phase differences of activity between the cortical regions. We previously reported phase advancement of bilateral auditory regions in comparison with the posterior regions, when we presented auditory stimuli to 3-month-old infants (Taga et al., 2011). The homologous connectivity between the frontal regions mostly showed a phase gradient from the left frontal regions to the right homologous regions (Fig. 3), although the reason for this gradient is not yet clear. The phase gradients of stimulus-driven activity and spontaneous activity in multiple infant groups of different ages, as well as child and adult groups, might clarify the temporal information of interhemispheric relationships. Functional lateralization can also be affected by intrahemispheric connectivity. Excitatory and inhibitory connectivity within a hemisphere facilitates and suppresses the specificity of the hemisphere, respectively. Therefore, the comparison of intrahemispheric connectivity between the hemispheres affords a clue to the details of lateralized organization. We previously reported that the left and right hemispheres of 3-month-old infants showed different patterns of coherence in fronto-posterior connectivity; the left hemisphere showed higher coherence in lower frequency bands when we measured fluctuations of brain activity after a 3 min speech-sound presentation (Homae et al., 2011). This previous study suggests distinct roles of the left and right networks, such that the right network is involved in retaining speech information, and the left network produces some representation that is relevant to speech information. The next question that should be answered is how these hemispheric-specialized processes interact with each other. I hope that future studies will reveal the relationships between intrahemispheric and interhemispheric connectivity, which forms at once differentiated systems, and a single unified system.

Fig. 3. An example of mutual synchronization of hemodynamic changes. The functional connectivity between homologous channels reported in Taga et al. (2011) is selectively depicted. The phase gradient from a phase-advanced channel to a phase-delayed channel is illustrated by a blue arrow (see detail, Taga et al., 2011). The black lines indicate the borderlines of four lobes, based on Watanabe et al. (2013). Interestingly, the majority of the left frontal channels showed phase advancement relative to the right homologous channels.

The simultaneous recording of NIRS and electroencephalography (EEG) will provide a new perspective into hemispheric relationships on multiple time scales. Telkemeyer et al. (2009, 2011) successfully applied such simultaneous recordings to neonates, 3-month-old infants, and 6-month-old infants. There have also been multiple studies performed using simultaneous recordings in adults (Herrmann et al., 2008; Horovitz and Gore, 2004; Kennan et al., 2002; Koch et al., 2008; Nasi et al., 2010; Obrig et al., 2002). Most of these compared the amplitudes of visual/auditory evoked potentials (VEPs/AEPs), or N400 with NIRS signals. Another way to make use of such simultaneous recordings would be to assess whether the cortico-cortical connectivity of multiple regions, including homologous connectivity revealed by NIRS is related to frequency-specific EEG powers. This comparison might reveal regionally dependent characteristics of homologous connectivity. The simultaneous NIRS–EEG will open a new window to investigate the hemispheric relationships of brain functions.

Conclusions In this review, I have focused on hemispheric relationships during spontaneous activity and functional activation. Considering the results of anatomical and functional connectivity studies on brain development, the origin of unilateral brain function observed in NIRS studies changes during development from the independence of local regions, to the mutual inhibition of homologous regions. Lateralized brain organization might influence the development of cognitive function, and vice versa. NIRS can provide insights into hemispheric and regional specialization, which forms the basis of perceptual and cognitive functions, including acoustic processing, facial processing, memory, emotion, and language. Multimodal measurements using multi-channel NIRS and EEGs and spatiotemporal analyses covering a wide age range of subjects will contribute greatly to progress in cognitive neuroscience.

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Acknowledgments The author wishes to thank G. Taga and H. Watanabe for their helpful discussions, and K. Asakawa for her administrative and technical assistance. This work was partly supported by Grants-in-Aid for Scientific Research (No. 24680044). Conflict of interest The author declares that there are no conflicts of interest.

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