Nonspatial processing

Nonspatial features of visual information are processed in the ventral visual pathway that proceeds from V1 through V2 and V4 to areas TEO and TE in the inferior temporal cortex and beyond. Consistent with the role of these areas in object recognition, neurons in V4, TEO and TE show response selectivities for stimulus attributes such as shape, color and texture (Desimone et al., 1984; Desimone and Schein, 1987; Gallant et al., 1993; Komatsu and Ideura, 1993; Kobatake and Tanaka, 1994).

Already in the 1970s Zeki (1973) found a functionally specialized area for color in V4 of the macaque monkey. In human brain imaging studies, color processing has been assigned to areas in the fusiform (FG) and lingual (LG) gyruses and collateral sulcus in the ventral occipitotemporal cortex (Lueck et al., 1989; McKeefry and Zeki, 1997; Hadjikhani et al., 1998) which are activated in tasks requiring either perception or attention to color (Corbetta et al., 1990;

Beauchamp et al., 1999). Therefore these areas have been postulated to be the human homologue of V4 of the monkey brain (Lueck et al., 1989; McKeefry and Zeki, 1997). Electrophysiological studies in monkeys have shown increased responses of V4 neurons to attended color stimuli (Haenny and Schiller, 1988) that become increasingly enhanced and selective as the difficulty level of a color discrimination task increases and thus requires more attention. The specialization of V4 for color processing was further supported by findings showing that lesions that produce cerebral color blindness, achromatopsia, seem to include this area (Zeki, 1990).However, there is

some discrepancy among the different studies in the cortical location and function of the color selective areas (Hadjikhani et al., 1998; Bartels and Zeki 2000; Zeki, 2003).

The crucial role of the ventral stream in object recognition is supported by deficits in this property found in brain damaged patients, for example patients with bilateral occipitotemporal lesions present object agnosia and are incapable of recognizing familiar faces (Farah, 1992).

Results of functional brain imaging studies in humans imply that object recognition is mediated by both distributed and localized representations in the ventral visual areas (Ishai et al., 1999;

Haxby et al., 2001; Spiridon and Kanwisher, 2002). Because objects of different categories activate wide areas of the ventral visual cortex, representation of objects appears to be more feature than object based in this cortical area. However, specialized regions of human ventral visual cortex have been shown to be dedicated to categories of high biological relevance such as faces (Kanwisher et al., 1997a), places (Epstein and Kanwisher, 1998) and bodies (Downing et al., 2001). In the monkey cortex, face selective cells have been found in the inferior temporal area and superior temporal sulcus (Desimone, 1991) and in the human brain, an area activated by face stimuli has been located in the FG of ventral occipitotemporal cortex (Kanwisher et al., 1997a;

McCarthy et al., 1997) and named as a fusiform face area (FFA). Tsao et al. (2003) demonstrated discrete face-selective patches of activation in an area extending from V4 to TE in macaque monkeys. These patches were similar in relative size and number to face patches in humans suggesting that humans and macaques share a similar brain architecture for visual object processing. A region in the human parahippocampal cortex has been shown to be more activated in response to complex scenes such as rooms, landscapes and city streets compared to objects, faces, houses or other kinds of visual stimuli (Epstein and Kanwisher, 1998; Epstein et al., 1999), and has been named as a parahippocampal place area. A region in the lateral occipital cortex that is activated more by photographs of human bodies and body parts than by various inanimate objects and object parts has been named as the extrastriate body area (Downing et al., 2001). Yet another region in lateral occipital cortex appears to respond to all objects regardless of meaning.

This region responds more strongly to pictures of objects than to textured patterns or degraded pictures of objects (Malach et al., 1995) and also to pictures of both real and nonsense objects to visual noise patterns or scrambled pictures of objects (Martin et al., 1996; Kanwisher et al., 1997b), and may thus be involved in form processing independent of object recognition.

2.2.2.2. Mnemonic information

WM processing of nonspatial information recruits a network of brain areas consisting of regions in the ventral visual pathway, especially in the inferior temporal cortex (IT) involved in the analysis of object features, and in the PFC areas indicated in the maintenance of object information. The IT is considered to have a role in maintaining nonspatial object information during the delay of a nonspatial WM task while the role of the PFC is currently unsettled (Curtis and D’Esposito, 2003; Postle, 2006b). Nonspatial WM related activity has been assigned to the VLPFC corresponding to BAs 45/47 in the human brain and to the inferior convexity of the monkey brain corresponding to Walker’s areas 12 and 45.

In monkeys, neurons in the inferior convexity have been shown to respond selectively to pictures of objects, and been involved in the processing of features and identity of objects (Goldman-Rakic, 1987; Wilson et al., 1993) such as faces (O’Scalaidhe et al., 1999) during WM task performance. Object-specificity of these neurons is further supported by the finding that their response to objects is not abolished by the presentation of distractive stimuli (Miller et al., 1996).

Furthermore, lesions of this area lead frequently to deficits in the performance of nonspatial WM tasks in monkeys (Goldman-Rakic, 1987). Neurons in the inferior convexity of the PFC are interconnected with neurons in the IT (Webster et al., 1994). Single-unit recordings in monkeys have shown that IT neurons express persistent, object-selective activity during the maintenance of visual objects across short delays (Miyashita and Chang, 1988; Miller et al., 1993; Nakamura and Kubota, 1995). The role of the IT in the maintenance of object information is further supported by studies that show serious impairments of WM processing of object features following inactivation (Fuster et al., 1981; Horel et al., 1987) or lesions (Petrides, 2000) of the IT.

Functional imaging studies in humans have shown activation of the PFC and IT during nonspatial tasks. Several studies have detected activation in the VLPFC suggesting a significant role for this area in nonspatial WM. Activation of this area has been indicated in studies using animate and non-animate objects (Ciesielski et al., 2006), faces (Courtney et al., 1997; Haxby et al., 2000; Sala et al., 2003), houses (Sala et al., 2003), object-based shapes (Ventre-Dominey et al., 2005) and color (Mohr et al., 2006) as memoranda. On the contrary, some authors have associated activity in this area more to specific top-down processes over the posterior cortical areas than to representation or storage of nonspatial information (Owen et al., 1998; D’Esposito et al., 1999, 2000; Owen, 2000; Postle, 2006a, b). However, several studies have localized an

area in the VLPFC that shows sustained activity in response to face stimuli (Courtney et al., 1997; Haxby et al., 2000; Sala et al., 2003). Similarly, a specific activation of the VLPFC during the performance of an object WM task has been found suggesting an involvement of the VLPFC in the maintenance of nonspatial information (Ventre-Dominey et al., 2005). However, the distribution of activation in the PFC by nonspatial mnemonic information may not be straightforward, but depend on the type of stimuli to be memorized. In one study, face stimuli that were considered to be more “pure” objects specifically activated the VLPFC but house stimuli that contained both spatial and nonspatial information induced activation that was distributed both to ventral and dorsal PFC regions (Sala et al., 2003).

Some fMRI studies suggest that visual WM is not mediated by the PFC but posterior cortical regions such as the IT involved in domain specific sensory processing (Postle and D’Esposito, 1999; Postle et al., 2000; Hautzel et al., 2002). The IT and occipital areas of the ventral visual pathway are persistently activated in nonspatial WM tasks. Maintaining geometrical shapes in WM were shown to activate areas in the FG, LG and IT (Postle and D’Esposito, 1999; Postle et al., 2000; Hautzel et al., 2002). Similarly, color processing in WM activated occipitotemporal areas corresponding to color-specific area V4 (Mohr et al., 2006).

Face processing in WM has been assigned to the FFA in the human brain (Courtney et al., 1997;

Druzgal and D’Esposito, 2001, 2003; Sala et al., 2003). Additionally, persistent FFA activity has been shown to increase linearly with the number of faces that are actively maintained in WM (Druzgal and D’Esposito, 2001, 2003) suggesting that this area is involved in maintaining and/or manipulating face information in WM. Furthermore, the load-dependent activation in these studies were shown both for the FFA and PFC but with a context-dependent shift in the onset of PFC activity relative to FFA activity suggesting a bottom-up flow of information at encoding which changes to top-down flow at retrieval. Studies employing TMS during nonspatial WM task performance have shown that bilateral TMS over temporal cortex selectively disrupts the performance of visual object task (Oliveri et al., 2001) and rTMS over VLPFC disrupts memory for faces (Mottaghy et al., 2002) thus providing support for the findings of fMRI and single-unit recording studies of the organization of nonspatial WM.