Elsevier

Neuropsychologia

Volume 47, Issue 3, February 2009, Pages 657-662
Neuropsychologia

Hemodynamic changes in the infant cortex during the processing of featural and spatiotemporal information

https://doi.org/10.1016/j.neuropsychologia.2008.11.014Get rights and content

Abstract

Over the last 20 years neuroscientists have learned a great deal about the ventral and dorsal object processing pathways in the adult brain, yet little is known about the functional development of these pathways. The present research assessed the extent to which different patterns of neural activation, as measured by changes in blood volume and oxygenation, are observed in infant visual and temporal cortex in response to events that involve processing of featural differences or spatiotemporal discontinuities. Infants aged 6.5 months were tested. Increased neural activation was observed in visual cortex in response to a featural-difference and a spatiotemporal-discontinuity event. In addition, increased neural activation was observed in temporal cortex in response to the featural-difference but not the spatiotemporal-discontinuity event. The outcome of this experiment reveals early functional specialization of temporal cortex and lays the foundation for future investigation of the maturation of object processing pathways in humans.

Introduction

Over the last 20 years a great deal of research has been conducted on the neural basis of object processing. Early studies conducted with non-human primates suggested that there are two main routes for visual object processing (De Yoe & Van Essen, 1988; Goodale & Milner, 1992; Livingstone & Hubel, 1988; Mishkin, Ungerleider, & Macko, 1983; Ungerleider & Mishkin, 1982). The ventral route originates from the parvocellular layers of the lateral geniculate nucleus (LGN) and projects from the primary visual cortex to the temporal cortex and mediates processing of visual features important for the recognition and identification of objects. The dorsal route originates from the magnocellular layers of the LGN and projects from the primary visual cortex to the parietal cortex and is important for the analysis of motion, depth, and location. More recent studies with non-human (Orban, Van Essen, & Fanduffel, 2004; Tanaka, 2000, Tootell et al., 2003; Tsunoda, Yamane, Nishizaki, & Tanifuji, 2001; Wang, Tanifuji, & Tanaka, 1998; Wang, Tanaka, & Tanifuji, 1996) and human (Bly & Kosslyn, 1997; Grill-Spector, Kourtzi, & Kanwisher, 2001; Grill-Spector et al., 1998, Haxby et al., 1991; Kourtzi & Kanwisher, 2001; Kraut, Hart, Soher, & Gordon, 1997) primates, using more sophisticated neuroimaging techniques, provide converging evidence for the functional distinction between these two pathways.

Although we now have extensive information about the neural correlates of object processing in the adult, little is known about the functional development of these pathways. Research conducted with infant monkeys suggests that the temporal cortex undergoes significant structural and neurophysiological development early in life (Bachevalier, Brickson, Hagger, & Mishkin, 1990; Rodman, Skelly, & Gross, 1991; Webster et al., 1991, Webster et al., 1995). Metabolic, neurophysiological, and neuroanatomical data obtained with human infants also reveals significant neural maturation during the first year (e.g., Braddick, Atkinson, & Wattam-Bell, 2003; Braddick & Atkinson, 2007; Chugani & Phelps, 1986; Conel, 1939–1967; De Haan & Nelson, 1999; Franceschini, Thaker, Themelis, Krishnamoorthy & Bortfeld, 2007; Gunn et al., 2002, Purpura, 1975). However, because there are a limited number of non-invasive techniques available to measure localized functional brain activation in infants, little is known about the functional consequences of neural maturation. Recent advances in optical imaging, including near-infrared spectroscopy (NIRS), now offer the opportunity to study functional activation in human infants.

In NIRS, near-infrared light is projected through the scalp and skull into the brain and the intensity of the light that is diffusely reflected is recorded. Typically, during cortical activation local concentrations of oxyhemoglobin (HbO2) increase, whereas concentrations of deoxyhemoglobin (HbR) decrease (Hoshi & Tamura, 1993; Jasdzewski et al., 2003, Obrig et al., 1996; Strangman, Franceschini, & Boas, 2003; Villringer & Dirnagl, 1995). From the summated change in HbO2 and HbR, the total change in hemoglobin (HbT) can be computed. Given that changes in HbT signal changes in regional cerebral blood flow (rCBF), having a measure of HbT is an important guide in the interpretation of NIRS data. While an increase in blood volume would result in an increase in HbO2 and HbR, an increase in blood flow results in an increase in HbO2 and a “washout” of HbR (i.e., an increase in relative concentration of HbO2 and a decrease in relative concentration of HbR).

Predicting and interpreting changes in HbO2 and HbR during cortical activation is not always straightforward, however. For example, an increase in rCBF (as indicated by HbT) produces an increase in HbO2 and a decrease in HbR. At the same time, an increase in oxygen consumption produces a decrease in HbO2 and an increase in HbR. Furthermore, the effect of these opposing mechanisms may be different in infants than adults (Hintz et al., 2001, Meek et al., 1998; Sakatani, Chen, Lichty, Zuo, & Wang, 1999). Hence it is important to remember that changes in relative concentrations of HbO2 and HbR are produced by changes in blood volume, rCBF, and oxygen consumption and that the relation between these can be complex.

To capitalize on changes in HbO2 and HbR, near-infrared light between approximately 650 and 950 nm is utilized. At these wavelengths, light is differentially absorbed by oxygenated and deoxygenated blood (Gratton, Sarno, Maclin, Corballis, & Fabiani, 2000; Villringer & Chance, 1997). Measuring the light intensity modulation during stimulus presentation, and comparing it to the light intensity during a baseline event in which no stimulus is presented, provides important information about the hemodynamic response to brain activation.

Recently, researchers have successfully applied NIRS technology to human infants in the experimental setting (e.g., Baird et al., 2002; Bortfeld, Wruck, & Boas, 2007; Pena et al., 2003; Taga, Asakawa, Maki, Konishi, & Koizumi, 2003; Wilcox et al., 2005, Wilcox et al., 2008). Most of these studies have focused on region specific hemodynamic changes in the neocortex during perceptual and cognitive tasks. For example, Wilcox et al. (2005) assessed hemodynamic changes in the visual and the temporal cortex during a visual object processing task. In this task, 6.5-month-olds saw an event in which a green ball and a red box emerged successively to opposite sides of screen (Fig. 1A). Behavioral studies (Wilcox and Baillargeon, 1998a, Wilcox and Baillargeon, 1998b; Wilcox & Chapa, 2002) indicate that 4.5–11.5-month-old infants use the featural differences to interpret the event as involving two distinct objects. Analysis of the NIRS data revealed a significant increase in HbO2 in visual and temporal cortex during the test event. Follow-up studies replicated and extended these findings to other events involving featurally distinct objects (Wilcox et al., 2008) and demonstrated that activation is observed in visual but not temporal cortex in response to control events (e.g., when the same object is seen to both sides of the screen). These data suggest that object processing is functionally localized: whereas visual cortex responds to all events involving visual objects temporal cortex responds only when the objects differ in their featural properties.

What these findings leave open to speculation, however, is the extent to which temporal cortex mediates the processing of other types of object information. For example, in adults the ventral pathway mediates processing of object features but does not typically mediate processing of the spatiotemporal properties of objects. If the ventral pathway in the infant is organized in a way similar to that of the adult, then a different pattern of activation should be observed in temporal cortex in response to events involving analysis of object features than to events involving analysis of spatiotemporal information. The present research tests this hypothesis. Infants aged 6.5 months were presented with the featural-difference event of Wilcox et al. (2005; Fig. 1A) and a spatiotemporal-discontinuity event (Fig. 1B) and NIRS data were collected. Behavioral studies have demonstrated that infants 3.5 months and older interpret the spatiotemporal-discontinuity event as involving two objects (Schweinle & Wilcox, 2004; Wilcox & Schweinle, 2003).

Section snippets

Participants

Twelve 6.5-month-olds, 8 M (M age = 6 months, 15 days, range = 5 months, 12 days to 7 months, 11 days). Twelve additional infants were tested but eliminated from analysis because they failed to contribute usable NIRS data (e.g., large motion artifacts and/or poor signal-to-noise ratio). Seven infants saw the featural-difference event first.

Apparatus, stimuli, and procedure

Infants sat on a parent's lap facing a puppet-stage apparatus. The green ball used in the featural-difference event was 10.25 cm in diameter with colored dots. The

Looking time data

The infants looked almost continuously throughout the test trials (featural-difference, M = 27.62, S.D. = 1.85 and speed-discontinuity, M = 26.74, S.D. = 1.46) suggesting that they found the test events engaging.

NIRS data

The hemoglobin concentration response curves are shown in Fig. 2. In the featural-difference condition, relative changes in HbO2 and HbR concentration from 5 to 30 s following initiation of the event were compared to baseline. The first emergence of the box occurred at 3 s and, allowing 2 s for

Discussion

The present research used near-infrared spectroscopy to assess neural activation, as measured by changes in blood volume and oxygenation, in visual and temporal cortex in 6.5-month-olds during two object processing tasks, one that involved analysis of object features and the other that required analysis of spatiotemporal information.

As predicted, a hemodynamic response was observed in visual cortex (D1 and D2) in both conditions and the responses did not vary significantly by condition. At the

Acknowledgements

This research was supported by grants from the National Institutes of Health (HD48943 to T.W., HD46533 to H.B., and P41-RR14075 to D.B.). We would like to thank Tracy Smith and the undergraduate assistants in the Infant Cognition Laboratory at Texas A&M University for their help with data collection and the parents who so graciously agreed to have their infants participate in the research.

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