Allocentric Processing along the Ventral

Object Specificity in Lateral Temporal Cortices

Within the ventral pathway, visual information passes areas V1/V2 to ventral aspects of area V3 and extrastriate area V4, as well as MT+, with further inter- connections to superior and inferior temporal cortex (Barbas & Blatt, 1995; Fuster, 2008; Miller, Li, & Desimone, 1993; Miyashita, 1993; Ranganath, Co- hen, Dam, & D'Esposito, 2004; Wilson, Scalaidhe, & Goldman-Rakic, 1993; Wilson & McNaughton, 1993) (see also Figure 1.5). Neural selectivity for high- ly specific complex objects such as hands or faces gradually increases from early visual areas to later ventral areas, particularly for neurons in inferior temporal cortex (Desimone, Albright, Gross, & Bruce, 1984; Kanwisher, McDermott, & Chun, 1997; Malach, Reppas, Benson, Kwong, Jiang, Kennedy, Ledden, Brady, Rosen, & Tootell, 1995; Tanaka et al., 1993). Neural firing of these cells has been found to be exclusively determined by intrinsic figural and surface properties of objects, and not by self-to-object properties such as rela- tive location (Kobatake & Tanaka, 1994; Perrett, Smith, Potter, Mistlin, Head, Milner, & Jeeves, 1984, 1985; Tanaka, Saito, Fukada, & Moriya, 1991). These neurons reveal large receptive fields covering the fovea and extending into both visual hemifields, therefore allowing for object recognition as well as ob- ject generalization across several viewing perspectives (Milner & Goodale, 1996). In other words, lateral temporal structures support the construction of object representations that remain stable as the observing subject moves along trough the environment.

Place Cell Coding in Hippocampal Structures

Lateral temporal areas are closely interlinked with dorsolateral, ventrolateral and anterior prefrontal cortices, as well as medial temporal structures, particu- larly parahippocampal gyrus and hippocampus5. Neurons in the hippocampus of the rat, so-called ‘place cells’, have been characterized by their location- specific firing as the animal traverses the environment (Foster, Castro, & McNaughton, 1989; Maaswinkel, Jarrard, & Whishaw, 1999; McNaughton,

5 _{There are also connections from inferior temporal cortex to the amygdala, primarily asso-} ciated with learning processes (stimulus-response) in social and emotional contexts (Gaffan, Gaffan, & Harrison, 1988), which will not be considered further.

Barnes, Gerrard, Gothard, Jung, Knierim, Kudrimoti, Qin, Skaggs, Suster, & Weaver, 1996; Wilson & McNaughton, 1993).

Comparable neurons have been discovered in non-human primates (Georges- Francois, Rolls, & Robertson, 1999; Rolls, 1999) as well as in human epileptic patients (Ekstrom, Kahana, Caplan, Fields, Isham, Newman, & Fried, 2003; Hartley, Maguire, Spiers, & Burgess, 2003; Iaria, Chen, Guariglia, Ptito, & Pe- trides, 2007; Iaria, Petrides, Dagher, Pike, & Bohbot, 2003). Place cells fire maximally when the subject moves into a distinct region of the environment, i.e., the ‘place field’, and display virtually no activity in other areas.

Spatial coding of these cells is independent of the subject’s current orientation as well as stimuli available at a certain place. Instead, place cells code view- point-independently for the position of the subject itself in a space-fixed allo- centric reference frame (Georges-Francois et al., 1999; Matsumura, Nishijo, Tamura, Eifuku, Endo, & Ono, 1999; O'Keefe & Nadel, 1978; Rolls, 1999; White & McDonald, 2002; Wilson & McNaughton, 1993). Environment-based encod- ing provides the prerequisite for an enduring map-like representation of the environment that can be flexibly retrieved and allow for place recognition whenever re-encountering the same environment from different viewpoints (Maguire, Burgess, Donnett, Frackowiak, Frith, & O'Keefe, 1998a; Milner & Goodale, 1996; Muller, 1996; Squire, Stark, & Clark, 2004; Wolbers & Büchel, 2005). Based on these findings, hippocampal structures as well as lin- gual/posterior parahippocampal areas play a crucial role for the construction of an enduring spatial representation within an allocentric reference frame from episodic memory (Bohbot, Iaria, & Petrides, 2004; Bohbot, Kalina, Ste- pankova, Spackova, Petrides, & Nadel, 1998; Burgess, Maguire, & O'Keefe, 2002; Ekstrom et al., 2003; Epstein, Parker, & Feiler, 2007; Fowler, Saling, Conway, Semple, & Louis, 2002; Lambrey, Amorim, Samson, Noulhiane, Has- boun, Dupont, Baulac, & Berthoz, 2008; Maguire, Burgess, & O'Keefe, 1999; McCarthy, Evans, & Hodges, 1996; Smith & Mizumori, 2006; van Asselen et al., 2006; Wolbers & Büchel, 2005). Neuropsychological studies on humans also associated lesions within the ventral pathway with deficits in viewpoint- independent allocentric processing of spatial structures, termed ‘landmark ag- nosia’, as well as impaired ability in constructing new environmental represen- tations, so-called ‘anteriograde topographical disorientation’ (Aguirre & D'Es- posito, 1999; Turriziani, Carlesimo, Perri, Tomaiuolo, & Caltagirone, 2003). In a study of Maguire and colleagues (Maguire, Burke, Phillips, & Staunton, 1996), patients with lesions in either right or left temporal lobes were provided with videotape presentations of overlapping routes. Interestingly, both right and left lesion groups were comparably impaired on topographical orientation tasks, i.e., landmark recognition and sketch map drawing. However, only pa- tients with lesions in the right hippocampus made erroneous proximity judg- ments, whereas patients with lesions in the left hemisphere were commonly able to accomplish the task. Recent studies support the notion that particularly right hippocampal as well as parahippocampal structures are responsible for storing the locations of objects encountered in spatio-temporal sequence with-

Chapter 1 – Theoretical Framework in an enduring allocentric representation (Burgess, Maguire, Spiers, & O'Keefe, 2001; Ghaem et al., 1997; Gramann et al., 2006; Grön, Wunderlich, Spitzer, Tomczak, & Riepe, 2000; Johnsrude, Owen, Crane, Milner, & Evans, 1999; Parslow, Morris, Fleminger, Rahman, Abrahams, & Recce, 2005; van Asselen et al., 2006; Wolbers, Wiener, Mallot, & Büchel, 2007).