Emotion and location cues bias conceptual retrieval in people 1 with deficient semantic control 2

Visuo-spatial context and emotional valence are powerful cues to episodic retrieval, but the contribution of these inputs to semantic cognition has not been widely investigated. We examined the impact of visuo-spatial, facial emotion and prosody cues and miscues on the retrieval of dominant and subordinate meanings of ambiguous words. Cue photographs provided relevant visuo-spatial or emotional information, consistent with the interpretation of the ambiguous word being probed, while miscues were consistent with an alternative interpretation. We compared the impact of these cues in healthy controls and semantic aphasia patients with deficient control over semantic retrieval following left-hemisphere stroke. Patients showed greater deficits in retrieving the subordinate meanings of ambiguous words, and stronger effects of cueing and miscuing relative to healthy controls. These findings suggest that contextual cues that guide retrieval to the appropriate semantic information reduce the need to constrain semantic retrieval internally, while miscues that are not aligned with the task increase the need for semantic control. Moreover, both valence and visuo-spatial context can prime particular semantic interpretations, in line with theoretical frameworks that argue meaning is computed through the integration of these features. In semantic aphasia, residual comprehension relies heavily on facial expressions and visuospatial cues. This has important implications for patients, their families and clinicians when developing new or more effective modes of communication.

[1]  T. Rogers,et al.  Disorders of representation and control in semantic cognition: Effects of familiarity, typicality, and specificity , 2015, Neuropsychologia.

[2]  Anil F. Ramlackhansingh,et al.  Lesion identification using unified segmentation-normalisation models and fuzzy clustering , 2008, NeuroImage.

[3]  B. A. Conway,et al.  The effects of laforin, malin, Stbd1, and Ptg deficiencies on heart glycogen levels in Pompe disease mouse models , 2015 .

[4]  James L. McClelland,et al.  Concepts, Control, and Context: A Connectionist Account of Normal and Disordered Semantic Cognition , 2018, Psychological review.

[5]  E. Maguire,et al.  The Human Hippocampus and Spatial and Episodic Memory , 2002, Neuron.

[6]  I. Olson,et al.  Dissecting the uncinate fasciculus: disorders, controversies and a hypothesis. , 2013, Brain : a journal of neurology.

[7]  Weiwei Zhang,et al.  Mood-dependent retrieval in visual long-term memory: dissociable effects on retrieval probability and mnemonic precision , 2018, Cognition & emotion.

[8]  Tony W Buchanan,et al.  Retrieval of emotional memories. , 2007, Psychological bulletin.

[9]  A. Luria The Working Brain: An Introduction To Neuropsychology , 1976 .

[10]  A. Damasio,et al.  Lesion analysis in neuropsychology , 1989 .

[11]  P. Hoffman,et al.  Ventrolateral Prefrontal Cortex Plays an Executive Regulation Role in Comprehension of Abstract Words: Convergent Neuropsychological and Repetitive TMS Evidence , 2010, The Journal of Neuroscience.

[12]  Matthew H. Davis,et al.  The neural mechanisms of speech comprehension: fMRI studies of semantic ambiguity. , 2005, Cerebral cortex.

[13]  T. Rogers,et al.  The neural and computational bases of semantic cognition , 2016, Nature Reviews Neuroscience.

[14]  Max Coltheart,et al.  Psycholinguistic assessments of language processing in aphasia (PALPA) , 1996 .

[15]  Elizabeth Jefferies,et al.  Semantic Processing in the Anterior Temporal Lobes: A Meta-analysis of the Functional Neuroimaging Literature , 2010, Journal of Cognitive Neuroscience.

[16]  Elizabeth Jefferies,et al.  The Differential Contributions of pFC and Temporo-parietal Cortex to Multimodal Semantic Control: Exploring Refractory Effects in Semantic Aphasia , 2012, Journal of Cognitive Neuroscience.

[17]  Matthew A. Lambon Ralph,et al.  Differential Contributions of Bilateral Ventral Anterior Temporal Lobe and Left Anterior Superior Temporal Gyrus to Semantic Processes , 2011, Journal of Cognitive Neuroscience.

[18]  Elizabeth Jefferies,et al.  Exploring multimodal semantic control impairments in semantic aphasia: Evidence from naturalistic object use , 2009, Neuropsychologia.

[19]  Elizabeth Jefferies,et al.  Situating the default-mode network along a principal gradient of macroscale cortical organization , 2016, Proceedings of the National Academy of Sciences.

[20]  Kerrie E. Elston-Güttler,et al.  Native and L2 Processing of Homonyms in Sentential Context. , 2005 .

[21]  Elizabeth Jefferies,et al.  Deregulated Semantic Cognition Follows Prefrontal and Temporo-parietal Damage: Evidence from the Impact of Task Constraint on Nonverbal Object Use , 2011, Journal of Cognitive Neuroscience.

[22]  Elizabeth Jefferies,et al.  Charting the effects of TMS with fMRI: Modulation of cortical recruitment within the distributed network supporting semantic control , 2016, Neuropsychologia.

[23]  B L Miller,et al.  Patterns of brain atrophy in frontotemporal dementia and semantic dementia , 2002, Neurology.

[24]  Endel Tulving,et al.  Encoding specificity and retrieval processes in episodic memory. , 1973 .

[25]  Guy B. Williams,et al.  What the left and right anterior fusiform gyri tell us about semantic memory. , 2010, Brain : a journal of neurology.

[26]  N. Hazen,et al.  The Effect of Spatial Context on Young Children's Recall. , 1984 .

[27]  A. Drzezga,et al.  Cerebral metabolic patterns at early stages of frontotemporal dementia and semantic dementia. A PET study , 2004, Neurobiology of Aging.

[28]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[29]  Tim Shallice,et al.  The Hayling and Brixton Tests , 1997 .

[30]  J. Raven Coloured progressive matrices : sets A, Ab, B , 1956 .

[31]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[32]  L. Rapport,et al.  Validation of the Warrington theory of visual processing and the Visual Object and Space Perception Battery. , 1998, Journal of clinical and experimental neuropsychology.

[33]  Nico Papinutto,et al.  Structural connectivity of the human anterior temporal lobe: A diffusion magnetic resonance imaging study , 2016, Human brain mapping.

[34]  L. M. Schoen,et al.  Semantic flexibility and core meaning , 1988 .

[35]  Ingrid R. Olson,et al.  Social cognition and the anterior temporal lobes , 2010, NeuroImage.

[36]  Richard S. J. Frackowiak,et al.  A voxel‐based morphometry study of semantic dementia: Relationship between temporal lobe atrophy and semantic memory , 2000, Annals of neurology.

[37]  C. Davis N-Watch: A program for deriving neighborhood size and other psycholinguistic statistics , 2005, Behavior research methods.

[38]  J. Hodges,et al.  The Cambridge Semantic Memory Test Battery: Detection of semantic deficits in semantic dementia and Alzheimer's disease , 2010, Neurocase.

[39]  G. Bower Mood and memory. , 1981, The American psychologist.

[40]  Neil Burgess,et al.  The hippocampus, space, and viewpoints in episodic memory , 2002, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[41]  M. Moscovitch,et al.  The effects of spatial contextual familiarity on remembered scenes, episodic memories, and imagined future events. , 2014, Journal of experimental psychology. Learning, memory, and cognition.

[42]  Skyler T. Hawk,et al.  Presentation and validation of the Radboud Faces Database , 2010 .

[43]  A. Woollams,et al.  “L” is for tiger: Effects of phonological (mis)cueing on picture naming in semantic aphasia , 2009, Journal of Neurolinguistics.

[44]  G. Bower,et al.  In search of mood-dependent retrieval. , 1989 .

[45]  Elizabeth Jefferies,et al.  Shared neural processes support semantic control and action understanding , 2015, Brain and Language.

[46]  Ian H. Robertson,et al.  The test of everyday attention , 1994 .

[47]  G. Gainotti Old and recent approaches to the problem of non-verbal conceptual disorders in aphasic patients , 2014, Cortex.

[48]  Elizabeth Jefferies,et al.  Going beyond Inferior Prefrontal Involvement in Semantic Control: Evidence for the Additional Contribution of Dorsal Angular Gyrus and Posterior Middle Temporal Cortex , 2013, Journal of Cognitive Neuroscience.

[49]  M. L. Lambon Ralph,et al.  The Neural Organization of Semantic Control: TMS Evidence for a Distributed Network in Left Inferior Frontal and Posterior Middle Temporal Gyrus , 2010, Cerebral cortex.

[50]  Remco J. Renken,et al.  Semantic ambiguity processing in sentence context: Evidence from event-related fMRI , 2007, NeuroImage.

[51]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

[52]  Pascale Piolino,et al.  Anatomical and functional alterations in semantic dementia: A voxel-based MRI and PET study , 2007, Neurobiology of Aging.

[53]  Elizabeth Jefferies,et al.  The impact of semantic impairment on verbal short-term memory in stroke aphasia and semantic dementia: A comparative study. , 2008, Journal of memory and language.

[54]  Lars A. Ross,et al.  Social cognition and the anterior temporal lobes: a review and theoretical framework. , 2013, Social cognitive and affective neuroscience.

[55]  Paul Hoffman,et al.  Concrete versus abstract forms of social concept: an fMRI comparison of knowledge about people versus social terms , 2018, Philosophical Transactions of the Royal Society B: Biological Sciences.

[56]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[57]  C. Macdonald Audacity , 2011, PAJ: A Journal of Performance and Art.

[58]  Richard J. Binney,et al.  Mapping the Multiple Graded Contributions of the Anterior Temporal Lobe Representational Hub to Abstract and Social Concepts: Evidence from Distortion-corrected fMRI , 2016, Cerebral cortex.

[59]  Paul J. Harrison,et al.  Asymmetry of the uncinate fasciculus: a post-mortem study of normal subjects and patients with schizophrenia. , 2002, Cerebral cortex.

[60]  E. Eich Searching for Mood Dependent Memory , 1995 .

[61]  Stephen G. Gilligan,et al.  Emotional Mood as a Context for Learning and Recall. , 1978 .

[62]  J. Hodges,et al.  Non-verbal semantic impairment in semantic dementia , 2000, Neuropsychologia.

[63]  Elizabeth Jefferies,et al.  Elucidating the Nature of Deregulated Semantic Cognition in Semantic Aphasia: Evidence for the Roles of Prefrontal and Temporo-parietal Cortices , 2010, Journal of Cognitive Neuroscience.

[64]  M. L. Lambon Ralph,et al.  Semantic impairment in stroke aphasia versus semantic dementia: a case-series comparison. , 2006, Brain : a journal of neurology.

[65]  Morris Moscovitch,et al.  The spatial scaffold: The effects of spatial context on memory for events. , 2016, Journal of experimental psychology. Learning, memory, and cognition.

[66]  Elizabeth Jefferies,et al.  Exploring the role of the posterior middle temporal gyrus in semantic cognition: Integration of anterior temporal lobe with executive processes , 2016, NeuroImage.

[67]  Norbert Schuff,et al.  Deformation tensor morphometry of semantic dementia with quantitative validation , 2004, NeuroImage.

[68]  G. Gainotti A historical review of investigations on laterality of emotions in the human brain , 2018, Journal of the history of the neurosciences.

[69]  H. Head Aphasia and kindred disorders of speech , 1926 .

[70]  Elizabeth Jefferies,et al.  Different impairments of semantic cognition in semantic dementia and semantic aphasia: evidence from the non-verbal domain. , 2009, Brain : a journal of neurology.

[71]  Neil Burgess,et al.  A neural-level model of spatial memory and imagery , 2018, eLife.

[72]  E. Jefferies The neural basis of semantic cognition: Converging evidence from neuropsychology, neuroimaging and TMS , 2013, Cortex.

[73]  P. Dixon,et al.  University of Alberta norms of relative meaning frequency for 566 homographs , 1994, Memory & cognition.

[74]  S. Robinson,et al.  The Effect of Mood-Context on Visual Recognition and Recall Memory , 2010, The Journal of general psychology.

[75]  N. Dronkers,et al.  Toward a functional neuroanatomy of semantic aphasia: A history and ten new cases , 2017, Cortex.

[76]  Sylvia Vitello,et al.  Resolving Semantic Ambiguities in Sentences: Cognitive Processes and Brain Mechanisms , 2015, Lang. Linguistics Compass.

[77]  K. Patterson,et al.  Deficits of knowledge vs . executive control in semantic cognition : Insights from cued naming , 2008 .

[78]  S. Thompson-Schill,et al.  Putting concepts into context , 2016, Psychonomic bulletin & review.

[79]  Sylvia Vitello,et al.  Roles of frontal and temporal regions in reinterpreting semantically ambiguous sentences , 2014, Front. Hum. Neurosci..

[80]  Elizabeth Jefferies,et al.  Shared processes resolve competition within and between episodic and semantic memory: Evidence from patients with LIFG lesions , 2018, Cortex.

[81]  S. Thompson-Schill,et al.  Semantic adaptation and competition during word comprehension. , 2008, Cerebral cortex.

[82]  Morris Moscovitch,et al.  The Primacy of Spatial Context in the Neural Representation of Events , 2018, The Journal of Neuroscience.

[83]  Glyn W. Humphreys,et al.  When “happy” means “sad”: Neuropsychological evidence for the right prefrontal cortex contribution to executive semantic processing , 2007, Neuropsychologia.

[84]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

[85]  T. Rogers,et al.  Where do you know what you know? The representation of semantic knowledge in the human brain , 2007, Nature Reviews Neuroscience.

[86]  John A. King,et al.  Memory for events and their spatial context: models and experiments. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[87]  M. L. Lambon Ralph,et al.  Demonstrating the Qualitative Differences between Semantic Aphasia and Semantic Dementia: A Novel Exploration of Nonverbal Semantic Processing , 2013, Behavioural neurology.

[88]  Elizabeth Jefferies,et al.  Conceptual control across modalities: graded specialisation for pictures and words in inferior frontal and posterior temporal cortex , 2015, Neuropsychologia.

[89]  Elizabeth Jefferies,et al.  Varieties of semantic ‘access’ deficit in Wernicke’s aphasia and semantic aphasia , 2015, Brain : a journal of neurology.

[90]  R. Reitan Validity of the Trail Making Test as an Indicator of Organic Brain Damage , 1958 .

[91]  R. Poldrack,et al.  Dissociable Controlled Retrieval and Generalized Selection Mechanisms in Ventrolateral Prefrontal Cortex , 2005, Neuron.

[92]  J. Smallwood,et al.  Automatic and Controlled Semantic Retrieval: TMS Reveals Distinct Contributions of Posterior Middle Temporal Gyrus and Angular Gyrus , 2015, The Journal of Neuroscience.