The present survey develops a previous position paper, in which I suggested that the multimodal semantic impairment observed in advanced stages of semantic dementia is due to the joint disruption of pictorial and verbal representations, subtended by the right and left anterior temporal lobes, rather than to the loss of a unitary, amodal semantic system. The main goals of the present review are (a) to survey a larger set of data, in order to confirm the differences in conceptual representations at the level of the right and left hemispheres, (b) to examine if language-mediated information plays a greater role in left hemisphere semantic knowledge than sensory-motor information in right hemisphere conceptual knowledge, and (c) to discuss the models that could explain both the differences in conceptual representations at the hemispheric level and the prevalence of the left hemisphere language-mediated semantic knowledge over the right hemisphere perceptually based conceptual representations. 1. Introduction The construct of “semantic hub” has been proposed by Patterson et al. [1] and Lambon Ralph and Patterson [2] to identify a neural network, bilaterally supported by regions of the anterior temporal lobes (ATL), that should sustain the interactive activation of representations in all modalities and for all semantic categories. This construct was prompted by the observation of the selective loss of conceptual knowledge that can be observed in semantic dementia (SD) but has raised several empirical and theoretical objections. In a previous position paper [3], I have tried to evaluate if defects for items presented in every modality and across categories in SD necessarily point to an abstract-amodal format of the conceptual representations that are disrupted in this disease, or if alternative interpretations can be advanced. This problem is theoretically relevant, because the assumption of an abstract-amodal format of the conceptual representations is in keeping with cognitive models (e.g., [4–7]) that assume that semantic representations, accessed through structural descriptions, are stored in an abstract and propositional format. However, other models (e.g., [8–12]) refute the hypothesis of a unitary, abstract, and amodal semantic system and rather assume that conceptual knowledge is represented in the same format in which it has been constructed by the sensory-motor system. My conclusion, with respect to the abstract-amodal format of the conceptual representations disrupted in SD, counters a unitary system for two main reasons. The first was that the
References
[1]
K. Patterson, P. J. Nestor, and T. T. Rogers, “Where do you know what you know? The representation of semantic knowledge in the human brain,” Nature Reviews Neuroscience, vol. 8, no. 12, pp. 976–987, 2007.
[2]
M. A. Lambon Ralph and K. Patterson, “Generalization and differentiation in semantic memory,” Annals of the New York Academy of Sciences, vol. 1124, pp. 61–76, 2008.
[3]
G. Gainotti, “The format of conceptual representations disrupted in semantic dementia: a position paper,” Cortex, vol. 48, no. 5, pp. 521–529, 2012.
[4]
Z. W. Pylyshyn, “What the mind's eye tells the mind's brain: a critique of mental imagery,” Psychological Bulletin, vol. 80, no. 1, pp. 1–24, 1973.
[5]
J. Fodor, The Language of Thought, Harvard University Press, Cambridge, Mass, USA, 1975.
[6]
M. J. Riddoch, G. W. Humphreys, M. Coltheart, and E. Funnell, “Semantic systems or system? Neuropsychological evidence re-examined,” Cognitive Neuropsychology, vol. 5, no. 1, pp. 3–25, 1988.
[7]
K. Patterson and J. R. Hodges, “Semantic dementia: one window on the structure and organisation of semantic memory,” in Handbook of Neuropsychology, F. Boller and J. Grafman, Eds., vol. 2, pp. 313–333, Elsevier, North Holland, The Netherlands, 2nd edition, 2000.
[8]
D. A. Allport, “Distributed memory, modular systems and dysphasia,” in Current Perspectives in Dysphasia, S. K. Newman and R. Epstein, Eds., Churchill Livingstone, Edinburgh, UK, 1985.
[9]
R. Jackendoff, “On beyond Zebra: the relation of linguistic and visual information,” Cognition, vol. 26, no. 2, pp. 89–114, 1987.
[10]
L. W. Barsalou, “Perceptual symbol systems,” Behavioral and Brain Sciences, vol. 22, no. 4, pp. 577–609, 1999.
[11]
G. Gainotti, “What the locus of brain lesion tells us about the nature of the cognitive defect underlying category-specific disorders: a review,” Cortex, vol. 36, no. 4, pp. 539–559, 2000.
[12]
G. Gainotti, “Anatomical functional and cognitive determinants of semantic memory disorders,” Neuroscience and Biobehavioral Reviews, vol. 30, no. 5, pp. 577–594, 2006.
[13]
A. Paivio, Imagery and Verbal Processes, Holt, Rinehart, and Winston, New York, NY, USA, 1971.
[14]
A. Paivio, Mental Representations: A Dual Coding Approach, Oxford University Press, Oxford, UK, 1986.
[15]
G. Gainotti, “The categorical organization of semantic and lexical knowledge in the brain,” Behavioural Neurology, vol. 3, pp. 109–115, 1990.
[16]
E. M. Saffran and M. F. Schwartz, “Of cabbages and things: semantic memory from a neuropsychological perspective—a tutorial review,” Attention and Performance, vol. 25, pp. 507–536, 1994.
[17]
G. Gainotti, M. C. Silveri, A. Daniele, and L. Giustolisi, “Neuroanatomical correlates of category-specific semantic disorders: a critical survey,” Memory, vol. 3, no. 3-4, pp. 247–264, 1995.
[18]
L. L. Chao and A. Martin, “Representation of manipulable man-made objects in the dorsal stream,” NeuroImage, vol. 12, no. 4, pp. 478–484, 2000.
[19]
A. Martin, L. G. Ungerleider, and J. V. Haxby, “Category-specificity and the brain: the sensory-motor model of semantic representations of objects,” in The New Cognitive Neurosciences, M. S. Gazzaniga, Ed., MIT Press, Cambridge, Mass, USA, 2000.
[20]
A. Martin and L. L. Chao, “Semantic memory and the brain: structure and processes,” Current Opinion in Neurobiology, vol. 11, no. 2, pp. 194–201, 2001.
[21]
A. R. Damasio, “Time-locked multiregional retroactivation: a systems-level proposal for the neural substrates of recall and recognition,” Cognition, vol. 33, no. 1-2, pp. 25–62, 1989.
[22]
A. R. Damasio, “Category-related recognition defects as a clue to the neural substrates of knowledge,” Trends in Neurosciences, vol. 13, no. 3, pp. 95–98, 1990.
[23]
G. Arrigoni and E. de Renzi, “Constructional apraxia and hemispheric locus of lesion,” Cortex, vol. 1, pp. 170–197, 1964.
[24]
E. de Renzi and H. Spinnler, “Visual recognition in patients with unilateral cerebral disease,” Journal of Nervous and Mental Disease, vol. 142, no. 6, pp. 515–525, 1966.
[25]
E. de Renzi and H. Spinnler, “Impaired performance on color tasks in patients with hemispheric damage,” Cortex, vol. 3, pp. 194–217, 1967.
[26]
E. de Renzi, G. Scotti, and H. Spinnler, “Perceptual and associative disorders of visual recognition. Relationship to the side of the cerebral lesion,” Neurology, vol. 19, no. 7, pp. 634–642, 1969.
[27]
E. de Renzi, P. Faglioni, and G. Scotti, “Hemispheric contribution to exploration of space through the visual and tactile modality,” Cortex, vol. 6, no. 2, pp. 191–203, 1970.
[28]
E. de Renzi, Disorders of Space Exploration and Cognition, Wiley and Sons, New York, NY, USA, 1982.
[29]
E. De Renzi, The History of Neurosciences in Autobiographies, vol. 5, Elsevier, North Holland, The Netherlands, 2006.
[30]
M. Mion, K. Patterson, J. Acosta-Cabronero et al., “What the left and right anterior fusiform gyri tell us about semantic memory,” Brain, vol. 133, no. 11, pp. 3256–3268, 2010.
[31]
P. J. Whitehouse, “Imagery and verbal encoding in left and right hemisphere damaged patients,” Brain and Language, vol. 14, no. 2, pp. 315–332, 1981.
[32]
M. Grossman and M. Wilson, “Stimulus categorization by brain-damaged patients,” Brain and Cognition, vol. 6, no. 1, pp. 55–71, 1987.
[33]
G. Gainotti, A. Cappa, R. Perri, and M. C. Silveri, “Disorders of verbal and pictorial memory in right and left brain-damaged patients,” International Journal of Neuroscience, vol. 78, no. 1-2, pp. 9–20, 1994.
[34]
A. Nieto, R. Santacruz, S. Hernández, J. Camacho-Rosales, and J. Barroso, “Hemispheric asymmetry in lexical decisions: the effects of grammatical class and imageability,” Brain and Language, vol. 70, no. 3, pp. 421–436, 1999.
[35]
N. Shibahara and B. Lucero-Wagoner, “Access to perceptual and conceptual information in the left and right hemispheres,” Perceptual and Motor Skills, vol. 93, no. 3, pp. 649–658, 2001.
[36]
G. Thierry, A.-L. Giraud, and C. Price, “Hemispheric dissociation in access to the human semantic system,” Neuron, vol. 38, no. 3, pp. 499–506, 2003.
[37]
G. Thierry and C. J. Price, “Dissociating verbal and nonverbal conceptual processing in the human brain,” Journal of Cognitive Neuroscience, vol. 18, no. 6, pp. 1018–1028, 2006.
[38]
J. Hocking and C. J. Price, “Dissociating verbal and nonverbal audiovisual object processing,” Brain and Language, vol. 108, no. 2, pp. 89–96, 2009.
[39]
K. Acres, K. I. Taylor, H. E. Moss, E. A. Stamatakis, and L. K. Tyler, “Complementary hemispheric asymmetries in object naming and recognition: a voxel-based correlational study,” Neuropsychologia, vol. 47, no. 8-9, pp. 1836–1843, 2009.
[40]
C. R. Butler, S. M. Brambati, B. L. Miller, and M. L. Gorno-Tempini, “The neural correlates of verbal and nonverbal semantic processing deficits in neurodegenerative disease,” Cognitive and Behavioral Neurology, vol. 22, no. 2, pp. 73–80, 2009.
[41]
G. Pobric, E. Jefferies, and M. A. Lambon Ralph, “Amodal semantic representations depend on both anterior temporal lobes: evidence from repetitive transcranial magnetic stimulation,” Neuropsychologia, vol. 48, no. 5, pp. 1336–1342, 2010.
[42]
R. Vandenberghe, C. Price, R. Wise, O. Josephs, and R. S. Frackowiak, “Functional anatomy of a common semantic system for words and pictures,” Nature, vol. 383, no. 6597, pp. 254–256, 1996.
[43]
J. S. Snowden, J. C. Thompson, and D. Neary, “Knowledge of famous faces and names in semantic dementia,” Brain, vol. 127, no. 4, pp. 860–872, 2004.
[44]
M. Ikeda, K. Patterson, K. S. Graham, M. A. Lambon Ralph, and J. R. Hodges, “A horse of a different colour: do patients with semantic dementia recognise different versions of the same object as the same?” Neuropsychologia, vol. 44, no. 4, pp. 566–575, 2006.
[45]
R. S. Hurley, K. A. Paller, E. J. Rogalski, and M. Marsel Mesulam, “Neural mechanisms of object naming and word comprehension in primary progressive aphasia,” Journal of Neuroscience, vol. 32, no. 14, pp. 4848–4855, 2012.
[46]
M. M. Mesulam, C. Wieneke, R. Hurley et al., “Words and objects at the tip of the left temporal lobe in primary progressive aphasia,” Brain, vol. 136, no. 2, pp. 601–618, 2013.
[47]
J. S. Snowden, J. C. Thompson, and D. Neary, “Famous people knowledge and the right and left temporal lobes,” Behavioural Neurology, vol. 25, no. 1, pp. 35–44, 2012.
[48]
D. Howard and K. Patterson, Pyramis and Palm Trees: Access from Pictures and Words, Thames Valley Test Company, Bury St Edmunds, UK, 1992.
[49]
S. Bozeat, M. A. Lambon Ralph, K. Patterson, P. Garrard, and J. R. Hodges, “Non-verbal semantic impairment in semantic dementia,” Neuropsychologia, vol. 38, no. 9, pp. 1207–1215, 2000.
[50]
R. Lesser, “Verbal comprehension in aphasia: an English version of three Italian tests,” Cortex, vol. 10, no. 3, pp. 247–263, 1974.
[51]
G. Gainotti, C. Caltagirone, and G. Miceli, “Semantic disorders of auditory language comprehension in right brain-damaged patients,” Journal of Psycholinguistic Research, vol. 8, no. 1, pp. 13–20, 1979.
[52]
G. Gainotti, C. Caltagirone, and A. Ibba, “Semantic and phonemic aspects of auditory language comprehension in aphasia,” Linguistics, vol. 13, no. 154-155, pp. 15–29, 1975.
[53]
G. Gainotti, C. Caltagirone, G. Miceli, and C. Masullo, “Selective semantic-lexical impairment of language comprehension in right-brain-damaged patients,” Brain and Language, vol. 13, no. 2, pp. 201–211, 1981.
[54]
Y. Joanette and P. Goulet, “Criterion-specific reduction of verbal fluency in right brain-damaged right-handers,” Neuropsychologia, vol. 24, no. 6, pp. 875–879, 1986.
[55]
B. Neininger and F. Pulvermüller, “Word-category specific deficits after lesions in the right hemisphere,” Neuropsychologia, vol. 41, no. 1, pp. 53–70, 2003.
[56]
G. Gainotti, G. Miceli, and C. Caltagirone, “The relationship between type of naming error and semantic-lexical discrimination in aphasic patients,” Cortex, vol. 17, no. 3, pp. 401–409, 1981.
[57]
D. O. Hebb, The Organization of Behaviour: A Neurophysiological Theory, Wiley and Sons, Hoboken, NJ, USA, 1949.
[58]
M. Friedrich and A. D. Friederici, “Phonotactic knowledge and lexical-semantic processing in one-year-olds: brain responses to words and nonsense words in picture contexts,” Journal of Cognitive Neuroscience, vol. 17, no. 11, pp. 1785–1802, 2005.
[59]
A. Majid, M. Bowerman, S. Kita, D. B. M. Haun, and S. C. Levinson, “Can language restructure cognition? The case for space,” Trends in Cognitive Sciences, vol. 8, no. 3, pp. 108–114, 2004.
[60]
J. G. Chi, E. C. Dooling, and F. H. Gilles, “Left right asymmetries of the temporal speech areas of the human fetus,” Archives of Neurology, vol. 34, no. 6, pp. 346–348, 1977.
[61]
S. de Schonen and E. Mathivet, “First come, first served : a scenario about the development of hemispheric specialization in face recognition during infancy,” European Bulletin of Cognitive Psychology, vol. 9, pp. 3–44, 1989.
[62]
C. Chiron, I. Jambaque, R. Nabbout, R. Lounes, A. Syrota, and O. Dulac, “The right brain hemisphere is dominant in human infants,” Brain, vol. 120, no. 6, pp. 1057–1065, 1997.
[63]
A. Franklin, G. V. Drivonikou, A. Clifford, P. Kay, T. Regier, and I. R. L. Davies, “Lateralization of categorical perception of color changes with color term acquisition,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 47, pp. 18221–18225, 2008.
[64]
G. Gainotti, F. Ciaraffa, M. C. Silveri, and C. Marra, “Mental representation of normal subjects about the sources of knowledge in different semantic categories and unique entities,” Neuropsychology, vol. 23, no. 6, pp. 803–812, 2009.
[65]
P. Hoffman and M. A. Lambon Ralph, “Shapes, scents and sounds: quantifying the full multi-sensory basis of conceptual knowledge,” Neuropsychologia, vol. 51, no. 1, pp. 14–25, 2013.
[66]
G. Gainotti, P. Spinelli, E. Scaricamazza, and C. Marra, “The evaluation of sources of knowledge underlying different semantic categories,” Frontiers in Human Neuroscience, vol. 7, article 40, 2013.