Developmental specificity of visual functions in humans

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We now have powerful brain imaging methods to study aspects of the physiology of sensory and language processing in humans. Event-related brain potentials (ERPs) and functional magnetic resonance imaging (fMRI) are two such techniques. ERPs are voltage fluctuations in the EEG in response to a controlled stimulus. The latencies of different positive and negative components in an ERP reveal the time course of activation (within microseconds) of the neuronal populations that are recruited during the processing of that stimulus. The fMRI technique measures changes in blood flow and oxygenation, permitting mapping of brain regions metabolically active following the presentation of a controlled stimulus. In contrast to the ERP, this technique has a good spatial resolution (about 1 mm) but a restricted temporal resolution.

Dorsal and Ventral Visual Subsystems In several experiments employing ERPs, we have observed that sensory and attentional processing of visual information presented to the central and peripheral visual fields elicit activity in different neural pathways in normal hearing subjects. Congenital auditory deprivation is associated with specific enhancements of behavioral performance and ERPs in response to visual information presented in the peripheral (but not the foveal) visual fields (Neville, Schmidt, and Kutas, 1983; Neville and Lawson, 1987a, b, c). These data suggest that the systems mediating the representation of peripheral visual space may be more modifiable than those representing central visual space. There is anatomical evidence that the visual periphery is represented most strongly along the dorsal visual pathway that projects from V1 toward the posterior parietal cortex and includes areas important for the processing of spatial location and motion information. By contrast, central space is largely represented along the ventral pathway that projects from V1 to anterior regions of the inferior temporal lobe and includes areas important for processing form and color information (Ungerleider and Mishkin, 1982; Baizer, Ungerleider, and Desimone, 1991). These results prompted the hypothesis that there may be a greater sensitivity to altered experience for other dorsal visual pathway functions.

In order to investigate this hypothesis, we employed stimuli designed to selectively activate either the magno-cellular system (M stimuli) which projects strongly to the dorsal pathway, or the parvocellular system which projects strongly (but not solely: see Stoner and Albright, 1993; Sawatari and Callaway, 1996) to the ventral pathway (P stimuli). The parvo system is highly responsive to color information and to stimuli of high spatial frequency, while the magno system is highly responsive to motion and to stimuli of low spatial frequency and low contrast (Livingstone and Hubel, 1988; Merigan and Maunsell, 1993).

Stimuli were presented at five different locations including the fovea and 8 degrees from the foveal stimulus in the upper and lower left and right visual fields. The parvo (P) stimuli were isoluminant blue and green high spatial frequency gratings (adjusted for the cortical magnification factor) continuously visible at all locations. ERPs were evoked by a brief change in color; randomly at one location the blue bars changed to red for 100 ms. The magno (M) stimuli consisted of low spatial frequency gratings of light and dark gray bars with a low luminance contrast. The evoking stimulus consisted of the bars at one location (random) moving transversely to the right. Subjects fixated centrally and monitored all locations for the rare occurrence of a black square at one of the locations. We first asked whether ERPs to these different stimuli would provide evidence for the activation of distinct neural systems in normal hearing subjects and then asked whether congenital auditory deprivation would have selective effects on these different aspects of processing (Armstrong et al., 1995; Neville and Bavelier, 1998).

In normal hearing subjects the distribution of the ERPs elicited by the parvo and magno stimuli displayed many similarities, and this may be attributable to the spatial proximity (within 1 cm) of the ventral and dorsal stream areas in humans, as indicated in recent fMRI studies (Sereno et al., 1995; Tootell et al., 1995). On the other hand, there were reliable differences in the activity patterns elicited by the stimuli. Magno stimuli elicited responses that were larger dorsally than were responses to parvo stimuli, consistent with our initial hypotheses. Additionally, both the current source density maps and the grand averaged waveforms demonstrate that, whereas the peripheral M stimuli elicited ERPs largest over cortex contralateral to the field of presentation, the P stimuli evoked a bilateral response. This pattern of results may be attributable in part to the deep ventrome-dial location of V4 which could generate a bilateral pattern of activation. Area MT, on the other hand, is located more laterally and would therefore generate a stronger contralateral response. Thus, these differences are consistent with anatomical differences of ventral and dorsal stream areas.

In addition, magno stimuli elicited ERP responses with considerably earlier latencies than those elicited by parvo stimuli, consistent with evidence from animal studies that show faster conduction within the magnocel-lular pathway. In addition, for several early components (beginning at 110 ms), P stimuli presented in the upper and lower visual fields (VF) evoked different response amplitudes while magno stimuli did not. These results may be accounted for by the retinotopic organization of V4 and MT/MST. fMRI data from humans (Sereno et al., 1995) have shown that upper and lower VF representations in several ventral stream areas including V4 are centimeters apart; however, in areas MT and MST, the representations are adjacent. Thus, a difference in response to parvo stimuli in the upper and lower VF is consistent with ventral stream activation, and the similarity of responses to magno stimuli in the upper and lower VF is consistent with dorsal stream activation. In summary, these stimuli were successful in evoking distinct ERP responses that may index the activation of separate streams or modes of visual processing in normal hearing subjects.

Effects of Auditory Deprivation Our prior research, coupled with evidence that different systems within vision display different developmental time courses and modification by visual experience (Sherman, 1985), led us to hypothesize that processing of the magno stimuli would be selectively enhanced in congen-itally deaf subjects.

Subjects were 11 congenitally, profoundly and bilaterally deaf subjects born to deaf parents. Whereas hearing subjects' reaction times were faster to targets occurring in the central than in the peripheral visual field, deaf subjects responded equally quickly to targets in the central and peripheral fields. Several specific group differences occurred in the amplitude and distribution of early sensory responses recorded over anterior and temporal regions. Deaf subjects displayed significantly greater amplitudes than hearing subjects-but this effect occurred only for magno stimuli, not for parvo stimuli (see figure 7.2). Further, whereas in hearing subjects, P stimuli elicited larger responses than did M stimuli, in deaf subjects responses to M stimuli were as large as those to P stimuli. In addition, at 150 ms ERPs to the M stimuli displayed a source-sink generator in temporal cortex that was clearly present in the deaf subjects but not in the hearing subjects. Currently, we are acquiring

FIGURE 7.2 ERPs elicited by (a) color change and (b) motion in normally hearing and congenitally deaf adults. Recordings from temporal and posterior temporal regions of the left and right hemispheres. (Reprinted with permission from Neville and Bavelier, 1998.)

FIGURE 7.2 ERPs elicited by (a) color change and (b) motion in normally hearing and congenitally deaf adults. Recordings from temporal and posterior temporal regions of the left and right hemispheres. (Reprinted with permission from Neville and Bavelier, 1998.)

results from a group of hearing subjects born to deaf parents who acquired ASL as a first language. This research should allow us to determine whether certain group effects observed in this experiment are attributable to auditory deprivation and others to acquisition of a visuospatial language (ASL) since, in previous research, we have observed separate effects of these two factors (Neville and Lawson, 1987c).

These data suggest that there is considerable specificity in the aspects of visual processing that are altered following auditory deprivation; specifically, the dorsal visual processing stream may be more modifiable in response to alterations in afferent input than is the ventral processing pathway. This hypothesis is in broad agreement with the proposal put forward by Chalupa and Dreher (1991) that components of the visual pathway that are specialized for high acuity vision exhibit fewer developmental redundancies ("errors"), decreased mod-ifiability, and more specificity than do those displaying less acuity and precision. It may also be that the dorsal visual pathway has a more prolonged maturational time course than the ventral pathway, permitting extrinsic influences to exert an effect over a longer time. While little evidence bears directly on this hypothesis, anatomical data suggest that, in humans, neurons in the parvocellu-lar layers of the LGN mature earlier than those in the magnocellular laminae (Hickey, 1977) and, in nonhuman primates, the peripheral retina is slower to mature (Lachica and Casagrande, 1988; Packer, Hendrickson, and Curcio, 1990; Van Driel, Provis, and Billson, 1990). Additionally, data suggest that the development of the Y-cell pathway (which is strongest in the periphery of

FIGURE 7.3 ERPs to auditory (speech) stimuli recorded over in children aged 6-36 months. (Reprinted with permission temporal and occipital regions in normal adults (bottom) and from Neville, 1995.)

the retina) is more affected by visual deprivation than is development of the W- and X-cell pathways (Sherman and Spear, 1982). Investigators have also reported that the effects of congenital visual deprivation (due to cataracts) are more pronounced on peripheral than foveal vision (and by implication on the dorsal pathway) (Mioche and Perenin, 1986; Bowering et al., 1997). Moreover, in developmental disabilities including dyslexia, specific language impairment, and Williams syndrome, visual deficits are more pronounced for dorsal than ventral visual pathway functions (Lovegrove, Garzia, and Nicholson, 1990; Eden et al., 1996; Atkinson et al., 1997). An additional hypothesis that may account for the greater effects on peripheral vision is that in development the effects of deprivation and enhancement are equivalent within all cortical regions. Those areas with less extent to begin with (e.g., MT, peripheral visual representations) would display the largest proportional effects of both enhancement and vulnerability. A similar hypothesis has been proposed to account for the larger effects of visual deprivation on ocular dominance formation within the periphery in monkeys (Horton and Hocking, 1997).

Sensitive Period Effects and Mechanisms We have observed that individuals who became deaf after the age of 4 years (due to delayed expression of the gene that leads to cochlear degeneration) typically do not display the increased visual ERPs that we attributed to auditory deprivation (Neville, Schmidt, and Kutas, 1983; Neville and Lawson, 1987c). We considered several mechanisms that might mediate the effects themselves and the developmental time limits on them. One possibility is that they are mediated by an early, normally transient, redundancy of connections between the auditory and visual systems (as has been observed in cats and hamsters: see Dehay, Bullier, and Kennedy, 1984; Frost, 1984; Inno-centi and Clarke, 1984). In the absence of competition from auditory input, visual afferents may be maintained on what would normally be auditory neurons. Our results from studies of later deafened individuals suggest that in humans this redundancy may diminish by the fourth year of life. One way we tested this hypothesis was to study the differentiation of visual and auditory sensory responses in normal development (see figure 7.3). In normal adults, auditory stimuli elicit ERP responses that are large over temporal brain regions but small or absent over occipital regions. By contrast, in 6-month-old children we observed that auditory ERPs are equally large over temporal and visual brain regions, consistent with the idea that there is less specificity and more redundancy of connections between auditory and visual cortex at this time. Between 6 and 36 months, however, we ob served a gradual decrease in the amplitude of the auditory ERP over visual areas, while the amplitude over the temporal areas was unchanged. These results suggest that early in human development there exists a redundancy of connections between auditory and visual areas and that this overlap gradually decreases between birth and 3 years of age. This loss of redundancy may be the boundary condition that determines when auditory deprivation can result in alterations in the organization of the visual system. Ongoing studies of hearing and deaf infants and children employing the parvo and magno stimuli described above will test for the specificity of these effects.

fMRI Study of Motion Perception We have further pursued the hypothesis that deafness alters the functional organization of the dorsal visual stream, by employing fMRI (Tomann et al., 1998). Specifically, we assessed whether early auditory deprivation alters cerebral activation during motion processing. in addition, we hypothesized that these changes would be most marked when visual attention was required in view of the central role of dorsal parietal regions in spatial attention. Motion processing was compared between congenitally deaf (native signers/born to deaf parents) and hearing individuals as visual attention was manipulated. Subjects fixated centrally and viewed an alternation of radial flow fields (converging and diverging) and static dots. While the first run required only passive viewing, visual attention was manipulated in all other runs by asking subjects to detect velocity and/or luminance changes.

Under conditions of active attention, deaf individuals showed a greater number of voxels activated and a larger percent signal change than did hearing subjects in temporal cortex including areas MT-MST (figure 7.4; see color plate 1). Thus, congenital deafness alters the cortical organization of motion processing, especially when attention is required. Interestingly, the recruitment of the intraparietal sulcus was also significantly larger in deaf than in hearing subjects. This result, like our earlier ERP study of spatial attention (Neville and Lawson, 1987b; Neville, 1995), suggests that early auditory deprivation may also alter the cortical organization of visual attention. ongoing studies will determine the precise location and the specificity of these effects.

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