The role of the right hemisphere in semantic control: A case-series comparison of right and left hemisphere stroke

Semantic control processes guide conceptual retrieval so that we are able to focus on non-dominant associations and features when these are required for the task or context, yet the neural basis of semantic control is not fully understood. Neuroimaging studies have emphasised the role of left inferior frontal gyrus (IFG) in controlled retrieval, while neuropsychological investigations of semantic control deficits have almost exclusively focussed on patients with left-sided damage (e.g., patients with semantic aphasia, SA). Nevertheless, activation in fMRI during demanding semantic tasks typically extends to right IFG. To investigate the role of the right hemisphere (RH) in semantic control, we compared nine RH stroke patients with 21 left-hemisphere SA patients, 11 mild SA cases and 12 healthy, aged-matched controls on semantic and executive tasks, plus experimental tasks that manipulated semantic control in paradigms particularly sensitive to RH damage. RH patients had executive deficits to parallel SA patients but they performed well on standard semantic tests. Nevertheless, multimodal semantic control deficits were found in experimental tasks involving facial emotions and the ‘summation’ of meaning across multiple items. On these tasks, RH patients showed effects similar to those in SA cases – multimodal deficits that were sensitive to distractor strength and cues and miscues, plus increasingly poor performance in cyclical matching tasks which repeatedly probed the same set of concepts. Thus, despite striking differences in single-item comprehension, evidence presented here suggests semantic control is bilateral, and disruption of this component of semantic cognition can be seen following damage to either hemisphere.

[1]  E. Warrington,et al.  Past, present, and prospects: Reflections 40 years on from the selective impairment of semantic memory (Warrington, 1975) , 2016, Quarterly journal of experimental psychology.

[2]  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.

[3]  A. Kasher,et al.  Effects of Right and Left Hemisphere Damage on Performance of the “Right Hemisphere Communication Battery” , 2002, Brain and Language.

[4]  Y. Joanette,et al.  Processing of metaphoric and non-metaphoric alternative meanings of words after right- and left-hemispheric lesion , 2003, Brain and Language.

[5]  Tim Shallice,et al.  Semantic access dysphasia resulting from left temporal lobe tumours , 2008, Brain : a journal of neurology.

[6]  Koji Jimura,et al.  Activation of Right Inferior Frontal Gyrus during Response Inhibition across Response Modalities , 2007, Journal of Cognitive Neuroscience.

[7]  Asa Kasher,et al.  Differential Effects of Right- and Left-Hemisphere Damage on Understanding Sarcasm and Metaphor , 2000 .

[8]  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.

[9]  David Badre,et al.  Left ventrolateral prefrontal cortex and the cognitive control of memory , 2007, Neuropsychologia.

[10]  Mia Liljeström,et al.  Perceiving and naming actions and objects , 2008, NeuroImage.

[11]  A. Wagner,et al.  Annals of the New York Academy of Sciences Cognitive Control and Right Ventrolateral Prefrontal Cortex: Reflexive Reorienting, Motor Inhibition, and Action Updating , 2022 .

[12]  J. Wambaugh,et al.  Contextual Constraint Treatment for coarse coding deficit in adults with right hemisphere brain damage: Generalisation to narrative discourse comprehension , 2015, Neuropsychological rehabilitation.

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

[14]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[15]  D. Plaut,et al.  The impact of synaptic depression following brain damage: A connectionist account of “access/refractory” and “degraded-store” semantic impairments , 2002, Cognitive, affective & behavioral neuroscience.

[16]  Geoffrey Donnan,et al.  Digital Map of Posterior Cerebral Artery Infarcts Associated With Posterior Cerebral Artery Trunk and Branch Occlusion , 2007, Stroke.

[17]  Denise Y. Harvey,et al.  Distinct loci of lexical and semantic access deficits in aphasia: Evidence from voxel-based lesion-symptom mapping and diffusion tensor imaging , 2015, Cortex.

[18]  Marco Bozzali,et al.  The differing roles of the frontal cortex in fluency tests. , 2012, Brain : a journal of neurology.

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

[20]  Richard J. Binney,et al.  The ventral and inferolateral aspects of the anterior temporal lobe are crucial in semantic memory: evidence from a novel direct comparison of distortion-corrected fMRI, rTMS, and semantic dementia. , 2010, Cerebral cortex.

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

[22]  S. Thompson-Schill,et al.  When lexical selection gets tough, the LIFG gets going: A lesion analysis study of interference during word production , 2005, Brain and Language.

[23]  Timothy J. Andrews,et al.  Responses in the right posterior superior temporal sulcus show a feature-based response to facial expression , 2015, Cortex.

[24]  N. Mashal,et al.  Conventionalisation of novel metaphors: A shift in hemispheric asymmetry , 2009, Laterality.

[25]  Niels O. Schiller,et al.  The nature of hemispheric specialization for linguistic and emotional prosodic perception: A meta-analysis of the lesion literature , 2011, Neuropsychologia.

[26]  E. Silberman,et al.  Hemispheric lateralization of functions related to emotion , 1986, Brain and Cognition.

[27]  A. Young,et al.  Configural information in facial expression perception. , 2000, Journal of experimental psychology. Human perception and performance.

[28]  K. Heilman,et al.  The role of the right hemisphere in emotional communication. , 1991, Brain : a journal of neurology.

[29]  Marco Bozzali,et al.  Verbal suppression and strategy use: a role for the right lateral prefrontal cortex? , 2015, Brain : a journal of neurology.

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

[31]  E. Warrington,et al.  A circumscribed refractory access disorder: A verbal semantic impairment sparing visual semantics , 2004, Cognitive neuropsychology.

[32]  E. Jefferies,et al.  Refractory effects in stroke aphasia: A consequence of poor semantic control , 2007, Neuropsychologia.

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

[34]  Wiltrud Fassbinder,et al.  Activation and maintenance of peripheral semantic features of unambiguous words after right hemisphere brain damage in adults , 2008, Aphasiology.

[35]  M. Schwartz,et al.  Semantic interference during blocked-cyclic naming: Evidence from aphasia , 2006 .

[36]  Emer M.E. Forde and Glyn W. Humphreys A semantic locus for refractory behaviour : Implications for access-storage distinctions and the nature of semantic memory , 1997 .

[37]  Elizabeth Jefferies,et al.  The use of cueing to alleviate recurrent verbal perseverations: Evidence from transcortical sensory aphasia , 2008 .

[38]  Mark Beeman,et al.  Coarse semantic coding and discourse comprehension. , 1998 .

[39]  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.

[40]  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.

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

[42]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex: one decade on , 2014, Trends in Cognitive Sciences.

[43]  L. Gauthier,et al.  The Bells Test: A quantitative and qualitative test for visual neglect. , 1989 .

[44]  Tim Shallice,et al.  Refractoriness and the healthy brain: A behavioural study on semantic access , 2011, Cognition.

[45]  Refractory semantic access dysphasia resulting from resection of a left frontal glioma , 2013, Neurocase.

[46]  Howard Gardner,et al.  Appreciation of metaphoric alternative word meanings by left and right brain-damaged patients , 1990, Neuropsychologia.

[47]  J. Duncan The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour , 2010, Trends in Cognitive Sciences.

[48]  D. Neary,et al.  Knowledge of famous faces and names in semantic dementia. , 2004, Brain : a journal of neurology.

[49]  Russell A. Poldrack,et al.  Inhibition-related Activation in the Right Inferior Frontal Gyrus in the Absence of Inhibitory Cues , 2011, Journal of Cognitive Neuroscience.

[50]  Carol A. Seger,et al.  Right hemisphere metaphor processing? Characterizing the lateralization of semantic processes , 2007, Brain and Language.

[51]  G. Humphreys,et al.  Asymmetrical white matter networks for attending to global versus local features , 2015, Cortex.

[52]  P. Hoffman,et al.  Selective short-term memory deficits arise from impaired domain-general semantic control mechanisms. , 2009, Journal of experimental psychology. Learning, memory, and cognition.

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

[54]  E. Warrington,et al.  Category specific access dysphasia. , 2002, Brain : a journal of neurology.

[55]  J. Duncan EPS Mid-Career Award 2004: Brain mechanisms of attention , 2006, Quarterly journal of experimental psychology.

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

[57]  P. Garthwaite,et al.  Point and interval estimates of effect sizes for the case-controls design in neuropsychology: Rationale, methods, implementations, and proposed reporting standards , 2010, Cognitive neuropsychology.

[58]  P. Marangolo,et al.  Metaphor Comprehension in Right Brain-Damaged Patients with Visuo-Verbal and Verbal Material: A Dissociation (RE)Considered , 2004, Cortex.

[59]  Randi C. Martin,et al.  Language Processing and Working Memory: Neuropsychological Evidence for Separate Phonological and Semantic Capacities , 1994 .

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

[61]  E. Warrington,et al.  CATEGORY SPECIFIC ACCESS DYSPHASIA , 1983 .

[62]  M. Faust,et al.  Cerebral hemispheric asymmetries in processing lexical metaphorsfn2 fn2 This research was part of the M.A. thesis of the first author at Bar-Ilan University under the supervision of the second author. , 1998, Neuropsychologia.

[63]  D. Maurer,et al.  The many faces of configural processing , 2002, Trends in Cognitive Sciences.

[64]  Matthew A. Lambon Ralph,et al.  Convergent Connectivity and Graded Specialization in the Rostral Human Temporal Lobe as Revealed by Diffusion-Weighted Imaging Probabilistic Tractography , 2012, Journal of Cognitive Neuroscience.

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

[66]  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.

[67]  M. Jung-Beeman Bilateral brain processes for comprehending natural language , 2005, Trends in Cognitive Sciences.

[68]  K. Bryan The Right Hemisphere Language Battery , 1995 .

[69]  James L. McClelland,et al.  No Right to Speak? The Relationship between Object Naming and Semantic Impairment:Neuropsychological Evidence and a Computational Model , 2001, Journal of Cognitive Neuroscience.

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

[71]  E. Jefferies,et al.  Deficits of semantic control produce absent or reverse frequency effects in comprehension: Evidence from neuropsychology and dual task methodology , 2012, Neuropsychologia.

[72]  ACTION CONCEPTS , 2002 .

[73]  A novel, implicit treatment for language comprehension processes in right hemisphere brain damage: Phase I data , 2011, Aphasiology.

[74]  K. Nakamura,et al.  Activation of the right inferior frontal cortex during assessment of facial emotion. , 1999, Journal of neurophysiology.

[75]  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.

[76]  Asa Kasher,et al.  Differential Effects of Right- and Left-Hemisphere Damage on Understanding Sarcasm and Metaphor , 2000 .

[77]  Geoffrey A. Donnan,et al.  A Digital Map of Middle Cerebral Artery Infarcts Associated With Middle Cerebral Artery Trunk and Branch Occlusion , 2005, Stroke.

[78]  John Duncan,et al.  The role of the right inferior frontal gyrus: inhibition and attentional control , 2010, NeuroImage.

[79]  D. E. Broadbent,et al.  Some Effects of Noise on Visual Performance , 1954 .

[80]  E. Warrington Quarterly Journal of Experimental Psychology the Selective Impairment of Semantic Memory the Selective Impairment of Semantic Memory , 2022 .

[81]  Michael Erb,et al.  Laterality in metaphor processing: Lack of evidence from functional magnetic resonance imaging for the right hemisphere theory , 2007, Brain and Language.

[82]  Jacqueline S. Laures-Gore,et al.  Performance of individuals with left hemisphere stroke and aphasia and individuals with right brain damage on forward and backward digit span tasks , 2011, Aphasiology.

[83]  Stewart H. Mostofsky,et al.  Response Inhibition and Response Selection: Two Sides of the Same Coin , 2008, Journal of Cognitive Neuroscience.

[84]  B. Kolb,et al.  Facial expression, emotion, and hemispheric organization , 2000 .

[85]  D. Neary Lesion Analysis in Neuropsychology , 1990 .

[86]  Timothy T Rogers,et al.  Semantic memory is impaired in patients with unilateral anterior temporal lobe resection for temporal lobe epilepsy. , 2012, Brain : a journal of neurology.

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

[88]  Mirella Dapretto,et al.  Metaphorical vs. literal word meanings: fMRI evidence against a selective role of the right hemisphere , 2006, NeuroImage.

[89]  P. Conn Neuroscience in Medicine , 2003, Humana Press.

[90]  P. Hoffman,et al.  The Roles of Left Versus Right Anterior Temporal Lobes in Conceptual Knowledge: An ALE Meta-analysis of 97 Functional Neuroimaging Studies , 2015, Cerebral cortex.

[91]  G. Dell,et al.  A Case-Series Test of the Interactive Two-Step Model of Lexical Access: Evidence from Picture Naming. , 2006 .

[92]  H. Gardner,et al.  The comprehension of metaphor in brain-damaged patients. , 1977, Brain : a journal of neurology.

[93]  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.

[94]  M. Phillips,et al.  Perception of emotions from faces and voices following unilateral brain damage , 2003, Neuropsychologia.

[95]  M. L. Lambon Ralph,et al.  Deregulated semantic cognition contributes to object-use deficits in Alzheimer's disease: A comparison with semantic aphasia and semantic dementia. , 2015, Journal of neuropsychology.

[96]  B. Sahakian,et al.  Differing patterns of temporal atrophy in Alzheimer’s disease and semantic dementia , 2001, Neurology.

[97]  Howard Gardner,et al.  Sensitivity to conversational deviance in right-hemisphere-damaged patients , 1992, Brain and Language.

[98]  K M Heilman,et al.  Differential impact of right and left hemisphere lesions on facial emotion and object imagery. , 1991, Brain : a journal of neurology.

[99]  R. Adolphs Neural systems for recognizing emotion , 2002, Current Opinion in Neurobiology.

[100]  Anjan Chatterjee,et al.  Action Concepts in the Brain: An Activation Likelihood Estimation Meta-analysis , 2013, Journal of Cognitive Neuroscience.

[101]  K. Heilman,et al.  The contribution of anterior and posterior regions of the right hemisphere to the recognition of emotional faces , 2009, Journal of clinical and experimental neuropsychology.

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

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

[104]  R. Galuske,et al.  Hemispheric asymmetries in cerebral cortical networks , 2003, Trends in Neurosciences.

[105]  Shari R. Baum,et al.  Unilateral brain damage effects on processing homonymous and polysemous words , 2005, Brain and Language.

[106]  Michal Lavidor,et al.  The Role of the Right Cerebral Hemisphere in Processing Novel Metaphoric Expressions: A Transcranial Magnetic Stimulation Study , 2008, Journal of Cognitive Neuroscience.

[107]  3D Angiographic Atlas of Neurovascular Anatomy and Pathology , 2007 .

[108]  Elizabeth Jefferies,et al.  Explaining semantic short-term memory deficits: Evidence for the critical role of semantic control , 2011, Neuropsychologia.

[109]  A. Kasher,et al.  Effects of Right- and Left-Hemisphere Damage on Understanding Conversational Implicatures , 1999, Brain and Language.

[110]  Karalyn Patterson,et al.  Taking both sides: do unilateral anterior temporal lobe lesions disrupt semantic memory? , 2010, Brain : a journal of neurology.

[111]  Roy W Jones,et al.  Comprehension of concrete and abstract words in semantic dementia. , 2009, Neuropsychology.

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

[113]  Page Widick,et al.  Functional–anatomical organization of predicate metaphor processing , 2008, Brain and Language.

[114]  J. Dien A tale of two recognition systems: Implications of the fusiform face area and the visual word form area for lateralized object recognition models , 2009, Neuropsychologia.

[115]  Roy W Jones,et al.  How does linguistic knowledge contribute to short-term memory? Contrasting effects of impaired semantic knowledge and executive control , 2012 .

[116]  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.

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

[118]  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.

[119]  N. Mashal,et al.  The role of the right cerebral hemisphere in processing novel metaphoric expressions taken from poetry: A divided visual field study , 2007, Neuropsychologia.

[120]  J. Grafman,et al.  Summation Priming and Coarse Semantic Coding in the Right Hemisphere , 1994, Journal of Cognitive Neuroscience.

[121]  E. Warrington,et al.  Word comprehension. The distinction between refractory and storage impairments. , 1996, Brain : a journal of neurology.

[122]  T. Shallice,et al.  Conceptual proposition selection and the LIFG: Neuropsychological evidence from a focal frontal group , 2010, Neuropsychologia.

[123]  D. Tranel,et al.  Behavioral patterns and lesion sites associated with impaired processing of lexical and conceptual knowledge of actions , 2012, Cortex.

[124]  Elizabeth A. Hirshorn,et al.  Localizing interference during naming: Convergent neuroimaging and neuropsychological evidence for the function of Broca's area , 2009, Proceedings of the National Academy of Sciences.

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

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

[127]  Christine Chiarello,et al.  Right hemisphere language comprehension : perspectives from cognitive neuroscience , 1998 .

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

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

[130]  Matthew A. Lambon Ralph,et al.  “W” is for bath: Can associative errors be cued? , 2011, Journal of Neurolinguistics.

[131]  C. Chiarello,et al.  Understanding metaphors: Is the right hemisphere uniquely involved? , 2007, Brain and Language.

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

[133]  Roy W Jones,et al.  The degraded concept representation system in semantic dementia: damage to pan-modal hub, then visual spoke. , 2012, Brain : a journal of neurology.

[134]  Thomas A. Schreiber,et al.  The University of South Florida free association, rhyme, and word fragment norms , 2004, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[135]  Sharon L. Thompson-Schill,et al.  Prefrontal Cortical Response to Conflict during Semantic and Phonological Tasks , 2007, Journal of Cognitive Neuroscience.

[136]  R. Giora Understanding figurative and literal language: The graded salience hypothesis , 1997 .

[137]  R. Leech,et al.  A functional network perspective on response inhibition and attentional control , 2014, Nature Communications.

[138]  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.

[139]  Daniel C. Krawczyk,et al.  Differences in task demands influence the hemispheric lateralization and neural correlates of metaphor , 2009, Brain and Language.

[140]  Matthew A. Lambon Ralph,et al.  Neurocognitive insights on conceptual knowledge and its breakdown , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[141]  Irene P. Kan,et al.  Verb generation in patients with focal frontal lesions: a neuropsychological test of neuroimaging findings. , 1998, Proceedings of the National Academy of Sciences of the United States of America.