Cortical activity during tactile exploration of objects in blind and sighted humans

“Before statistical analysis, standard preprocessing procedures were performed (see [10] and the Supplemental Information available online for detailed experimental procedures).”

“This evidence comes from observations that both congenitally blind and sighted individuals activate the LO cortex in response to sounds, but only if these individuals learn to extract geometrical shapes from those sounds such as when using a visual-to-auditory SSD or when using touch to recognize objects [67,78].”

“Amedi et al. (2010) found that tactile object identification activated visual object-recognition regions within LOC in blind individuals similarly as for sighted controls.”

“For example, it has been shown in early-blind adults that the recognition of tactile shapes (Amedi et al., 2010) activates the LOC/LOtv in a functionally selective crossmodal fashion.”

“Although there are many instances of plasticity observed in the visual system, for e.g. changes in V1 in individuals who are congenitally blind (Amedi et al., 2010), there has been rather little research on plasticity in higher-order areas of the cortical visual system (Das and Huxlin, 2010).”

“Another area well known for its functional specialization is the lateral-occipital complex (LOC), typically involved in object/form recognition processes, which has been shown on several occasions to be responsive to non-visual form processing in EB (Amedi et al., 2007, 2010).”

“Examples include lateral occipital cortex activation in response to tactile object recognition (Amedi et al., 2001, 2005, 2010; Pietrini et al., 2004); medial temporal area (MT) responses to perceived motion of non-visual stimuli (Hagen et al., 2002; Poirier et al., 2006; Ricciardi et al., 2007;…”

“Indeed, several groups investigated sensory substitution in blind subjects, trying to re-establish a sensory modality that has been lost by utilizing another one (Bach-y-Rita et al., 1998; Arno et al., 2001; Ptito et al., 2005; Renier et al., 2005; Amedi et al., 2010).”

“In striking contrast with this view, several studies suggested that the occipital cortex of congenitally blind people maintains a division of computational labor somewhat similar to the one characterizing the sighted brain (Amedi et al., 2010; Dormal and Collignon, 2011; Ricciardi et al., 2007).”

“when subjects performed tactile object recognition tasks [15].”

“frequently observed in individuals who are blind ([57]).”

“One consistent finding from these studies was evidence for a region in lateral occipital cortex (Amedi et al., 2002, 2007, 2010) that responds significantly more strongly to exploration of objects than to exploration of textures, to hand movements, or to retrieval of object knowledge (e.g.,…”

“Adapted from Amedi et al. 2007 Data adapted from Amedi et al. 2010 Data adapted from Amedi et al. 2001 RH Y = –59 Y = –58 Y = –57 Y = –71 Z = –7 Z = –9 Z = 9 LH LH RH RH”

“…order areas when it comes to more complex stimulation as for tactile or sound objects recognition and localization or the use of vision substitution devices (Amedi et al., 2002, 2010; Renier et al., 2010; StriemAmit et al., 2012b; Striem-Amit and Amedi, 2014), beyond basic sensory processing.”

“…Collignon et al., 2009; Gougoux et al., 2009; Röder et al., 1996), For example, blind individuals outperform sighted controls on tactile tasks (Amedi et al., 2010; Sadato et al., 1996), auditory tasks (Rauschecker, 1995; Röder et al., 1996), sound localization tasks (Collignon et al., 2009;…”

“In the blind the high demand required by object recognition appears to also recruit ventral and dorsal occipital areas [7].”

“Furthermore, increasing evidence has confirmed that CB subjects preserved functional organization in several higher-tier visual areas when performing non-visual sensory task, such as the dorsal stream specialized for spatial processing [25,26] and action control [27], the ventral stream for reading [28] and object rec…”

“For instance, the lateral-occipital complex (LOC), which responds to visual and tactile object shape in sighted [for a review see Lacey and Sathian, 2011], has been reported to respond during auditory shape processing in the blind [Amedi et al., 2007, 2010].”

“Cross-modal activations have been described in early and lateblind groups (Amedi et al., 2003, 2010; Buchel et al., 1998; Burton, 2003; Cheung et al., 2009; Merabet et al., 2007; Ptito et al., 2005; Sadato et al., 1996, 2004; Sathian, 2005).”

“The potential for plasticity of the visual system from blind patients is based on reported functional reorganizations after the onset of blindness [51,52].”

“been extensively reported in these subjects (Liu et al. 2007; Amedi et al. 2010; Bedny et al. 2011) or the preserved functional specialization in most brain areas (Mohan et al.”

“Additionally, assessment of responses in lower and higher tier visual areas from both hemispheres evaluated the hypothesis posed by Amedi and colleagues that left V1 particularly contributed to verbal recall processes (Amedi et al., 2003; Amedi et al., 2010; Raz et al., 2005).”

“Similar activation patterns with cross-modal responses extending posteriorly were reported in a previous study when congenitally blind participants performed a tactile recognition task (Amedi et al., 2010).”

“The reason is that reorganization of other processes, such as auditory motion perception and tactile object recognition, appears to follow the topography of the functionally equivalent visual processes in the sighted brain (Ricciardi et al., 2007a; Amedi et al., 2010; Dormal et al., 2016).”

“performed on trained subjects (blind or sighted), the motion of electrotactile shocks across the tongue activates the MT+ area of the visual cortex, an area which is normally involved in visual motion (Merabet et al., 2009; Amedi et al., 2010; Matteau et al., 2010).”

“…dorsal areas (e.g. Collignon et al., 2011; Renier et al., 2010), while the processing of auditory or tactile object identity has been found to activate ventral areas of the visual cortex in congenitally blind individuals (Amedi et al., 2007, 2010; Hölig et al., 2014; Pietrini et al., 2004).”

“For instance, born blind subjects, contrary to common beliefs, have never reported any color in their dreams or during hallucinatory states (Kiekopf, 1968; Raz et al., 2005; Amedi et al., 2010).”

“Studies in congenital blindness have repeatedly demonstrated the recruitment of these areas of the cortex for haptic processing 96 – 99 , underlining the integrative role of the structures of ventral pathway 100,101 .”

“This claim was also supported by sensory substitution devices (SSD) studies that the visual cortex was also involved in processing nonvisual tasks after a short period of SSD training in sighted subject [50, 72, 186].”

“[58] compared the patterns of activation generated by tactile object recognition tasks for eight sighted and congenitally blind subjects.”

“…impaired) activated the O2 (occipital lobe) channel in the generated tree. relevance of the brain signals in the occipital area can be derived from the idea presented in [19] that the activation of the occipital cortex often reflects the processing of mental visual images triggered by other senses.”

“For example, the lateral occipital complex (LOC), which is implicated in visual shape perception, is also active when blind individuals explore complex tactile shapes [59].”

“If these expectations are met, one might argue that tactile stimulation can, under certain circumstances, activate supramodal brain circuits (Amedi et al. 2010).”

“For instance, a strong correlation has been found between activation of V1 and performance on verbal memory and language-related tasks (Amedi et al., 2003).”

“One study found ILOTC’s activation when contrasting a haptic object recognition task and a task imitating the grasping and exploration of objects [22].”

“…versus animals (Mahon et al. 2009), tools (Peelen et al. 2013), or large objects (He et al. 2013), by manually exploring objects (Pietrini et al. 2004; Amedi et al. 2010), or by hearing the shape of objects or bodies via auditory substitution (Striem-Amit et al. 2012; Striem-Amit and Amedi 2014).”

“…and that haptic object recognition by touch or using visual-to-auditory substitution recruits the object related lateral occipital complex (LOC, Amedi et al., 2007, 2010), leading to the suggestion that this area is dedicated to deciphering the 3D shape of objects regardless of sensory…”

“Observing that individuals with VIs incorporate many tactile [4], [5]”

“Moreover, the existence of networks between vision and touch in normally sighted individuals is supported by neuroimaging studies; visual areas have been shown to be activated during tactile orientation discrimination (Sathian & Zangaladze, 2002; Sathian, Zangaladze, Epstein, & Grafton, 1999), haptic object recognitio…”

“For example, the occipital recruitment in blind people for tactile processing (Collignon et al., 2011; Amedi et al., 2010; Gougoux et al., 2005; Sathian, 2005; Hamilton & Pascual-Leone, 1998; Sadato et al., 1996) is explained as the request of the system to dedicate optimal processing to a modality that became critica…”

“, 2011), touch (Ptito et al., 2005, 2012; Amedi et al., 2010; Matteau et al., 2010) and audition (Gougoux et al.”

“, 2009; Amedi et al., 2010). In fact, they hold that the relevant finding for constraining models is not the format of the information that is represented but rather its organization. On the other hand, it can be objected that, to devise a task that could be performed by both sighted and blind individuals, Mahon et al…”

“Similarly, Amedi et al. (2010) had their subjects explore objects tactually using both hands.”

“after visual deprivation makes it responsive to a large variety of haptic and auditory tasks (Rosler et al. 1993; Roder et al. 1997; Burton et al. 2003; Ricciardi et al. 2007; Amedi et al. 2010; Dietrich et al. 2013; Lewald and Getzmann 2013; Occelli et al. 2013; Watkins et al. 2013; Striem-Amit and Amedi 2014; Anurov…”

“However, the same structure is strongly activated during somatosensory object recognition in people with blindess, suggesting that visual imagery is not an obligatory condition for tactile object recognition in visual cortex [3, 4, 21, 40] and others.”

“In blind subjects, the occipital cortex is activated during haptic (Amedi et al., 2010) and auditory (Kujala et al.”

“D objects and so is less likely to rely on a visual recoding, image mediation strategy to identify them (Lederman et al., 1990; see also Amedi et al., 2010).”

“This model is supported, at least prima facie , by evidence of cross-modal neuroplasticity of the “blind visual cortex” and its involvement in episodic memory [28], language [18], and in auditory [21,22,27,29] and haptic [30] processing [5].”

“Tactile discrimination studies have shown increased activation of posterior occipital areas when compared to their sighted counterparts [1, 2].”

“However, previous studies have found shared visuotactile representations of shape between both modalities (Amedi et al. 2010; Lacey et al. 2009).”

“…with claims that a supramodal or crossmodal object recognition system subserves both visual and haptic identification (Allen & Humphreys, 2009; Amedi et al., 2010; Lacey et al., 2009; Ricciardi & Pietrini, 2011) and extends it to include haptic inputs from invisible locations (behind the…”

“As well as, blind’s visual ventral stream activated during braille reading (Reich et al., 2011; StriemAmit et al., 2012; Abboud et al., 2015) and object recognition (Pietrini et al., 2004; Peltier et al., 2007;Mahon et al., 2009; Amedi et al., 2010; Striem-Amit and Amedi, 2014).”

“In contrast, evidence on LOC activation found in blind patients who could not exhibit visual imagery during haptic shape processing challenged the role of that particular area related to visual imagery (Amedi et al. 2010).”

“…( mm ) 0.5 0.0 similar functional region of cortex (i.e., LOtv) as indicated by other studies to be involved in visuohaptic object recognition (e.g., Amedi et al., 2001, 2002; Amedi et al., 2010; Kim et al., 2012), and provides an adequate proxy for LOC ROIs de fi ned using a more standardized task.”

“…to the environment and develop significant abilities resulting from changes that are made in the top-down and bottom-up interactions and related subcortical (Skoe and Kraus, 2010; Chandrasekaran et al., 2012) and cortical areas (Stevens and Weaver, 2009; Amedi et al., 2010; Focker et al., 2012).”

“Similar activation patterns with cross-modal responses extending posteriorly were reported in a previous study when congenitally blind participants performed a tactile recognition task (Amedi et al., 2010).”

“Although study includes a reasonable sample size, SCs (especially in adolescent group) could not be age matched, as it was difficult to recruit willing adolescents.”

“Cross-modal plasticity following the loss of visual inputs has been shown to give rise of tactile signals in primary visual cortex (Amedi et al., 2010; Merabet and Pascual-Leone, 2010; Van Brussel et al., 2011).”

“Third, we did not include the texture as a control when examining object preferences (e.g. James et al. 2002; Amedi et al. 2010).”

“…findings which show a large activation of Broca ' s network in CTB individuals and an increased functional long-range reciprocal connectivity be-tween this region and visual and frontal cortical areas (e.g., Alary et al., 2008; Amedi et al., 2010; Heine et al., 2015; Peltier et al., 2007).”

“activity appears more in temporo-occipital areas (ventral pathway) than parieto-occipital (dorsal pathway) ones (Amedi et al., 2010; Kandel & Wurtz, 2000), except at the end of the training period, when they are re-routed towards occipital areas.”

“…2014, Maidenbaum et al. 2014, Kupers and Ptito 2014) and many findings have accumulated supporting the principle for medium to high-level functions (e.g. Striem-Amit et al. 2012, Dormal et al. 2016, Peelen et al. 2013, Amedi et al. 2007, Amedi et al. 2010, Wolbers et al. 2011, Kitada et al. 2014).”

“While human guides can provide adaptive real-time feedback, they may compromise user autonomy [62].”

“Multimodal shape representation has been extensively studied at the object level (Amedi et al. 2001; Amedi et al. 2002; Amedi et al. 2007; Stilla and Sathian 2008; Lacey et al. 2009b; Amedi et al. 2010; Lacey and Sathian 2014; Lee Masson et al. 2016a).”

“In occipital cortex, blind would probably show effects throughout occipital cortex based on prior reports of activation with tactile stimulation in early blind (Amedi et al., 2010; Burton et al., 2004; © 2011 Elsevier B.V.”

“These findings were supported by Amedi et al. (2010), who showed that visual imagery is not an obligatory condition for object activation in visual cortex.”