Skip to main content
Top
Published in: Journal of Neurology 9/2013

01-09-2013 | Original Communication

The clinical and anatomical heterogeneity of environmental dependency phenomena

Authors: Julien Lagarde, Romain Valabrègue, Jean-Christophe Corvol, Isabelle Le Ber, Olivier Colliot, Marie Vidailhet, Richard Levy

Published in: Journal of Neurology | Issue 9/2013

Login to get access

Abstract

Following damage to the frontal lobes, the observation of patients presenting with environmental dependency syndrome (EDS), particularly with its two main components—grasping and imitation behavior, provides a unique opportunity to gain new insights into the neural bases of human autonomy and free-will. In the present study, thirty-nine patients with frontal lobe dysfunction [21 with progressive supranuclear palsy (PSP), and 18 with the behavioral variant of frontotemporal dementia, (bvFTD)] were tested for environmental dependency phenomena and underwent neuropsychological evaluation and T1-weighted 3D brain MRI. We correlated scores obtained by assessing grasping, imitation and utilization behaviors with both neuropsychological executive test performance and grey matter density on MRI using Voxel-Based Morphometry (VBM). This study confirms the high frequency of two environmental dependency phenomena- grasping and imitation- in patients with frontal lobe syndrome (34/39 patients) and the rarity of utilization behavior (2/39). The grasping score was significantly and positively correlated with those obtained in all executive tests except the Stroop test, while the imitation score was not. In the VBM study, while the grasping score was correlated with grey matter density in the right superior frontal gyrus and both inferior temporal gyri, the imitation score was correlated with changes in the right insula, left medial frontal gyrus and left precuneus. Environmental dependency is associated with the dysfunction of a frontoparietal network. Within this large network, grasping and imitation behaviors can be dissociated from both neuropsychological and anatomical standpoints, underlining the clinical and anatomical heterogeneity of environmental dependency phenomena.
Literature
1.
go back to reference Lhermitte F (1986) Human autonomy and the frontal lobes. Part II: patient behavior in complex and social situations: the “environmental dependency syndrome”. Ann Neurol 19:335–343PubMedCrossRef Lhermitte F (1986) Human autonomy and the frontal lobes. Part II: patient behavior in complex and social situations: the “environmental dependency syndrome”. Ann Neurol 19:335–343PubMedCrossRef
2.
go back to reference Goldberg E (2009) The new executive brain: frontal lobes in a complex world. Oxford University Press, New York Goldberg E (2009) The new executive brain: frontal lobes in a complex world. Oxford University Press, New York
3.
go back to reference Cambier J (1999) Loss of autonomy in humans: utilization and imitation behaviour. Rev Neurol (Paris) 155:879–883 Cambier J (1999) Loss of autonomy in humans: utilization and imitation behaviour. Rev Neurol (Paris) 155:879–883
4.
go back to reference Lhermitte F, Pillon B, Serdaru M (1986) Human autonomy and the frontal lobes. Part I: imitation and utilization behavior: a neuropsychological study of 75 patients. Ann Neurol 19:326–334PubMedCrossRef Lhermitte F, Pillon B, Serdaru M (1986) Human autonomy and the frontal lobes. Part I: imitation and utilization behavior: a neuropsychological study of 75 patients. Ann Neurol 19:326–334PubMedCrossRef
5.
go back to reference Shallice T, Burgess P, Schon P, Baxter D (1989) The origins of utilization behaviour. Brain 112:1587–1598PubMedCrossRef Shallice T, Burgess P, Schon P, Baxter D (1989) The origins of utilization behaviour. Brain 112:1587–1598PubMedCrossRef
6.
go back to reference Shimomura T, Mori E (1998) Obstinate imitation behaviour in differentiation of frontotemporal dementia from Alzheimer’s disease. Lancet 352:623–624PubMedCrossRef Shimomura T, Mori E (1998) Obstinate imitation behaviour in differentiation of frontotemporal dementia from Alzheimer’s disease. Lancet 352:623–624PubMedCrossRef
7.
go back to reference Ghosh A, Dutt A (2010) Utilisation behaviour in frontotemporal dementia. J Neurol Neurosurg Psychiatry 81:154–156PubMedCrossRef Ghosh A, Dutt A (2010) Utilisation behaviour in frontotemporal dementia. J Neurol Neurosurg Psychiatry 81:154–156PubMedCrossRef
8.
go back to reference De Renzi E, Cavalleri F, Facchini S (1996) Imitation and utilisation behaviour. J Neurol Neurosurg Psychiatry 61:396–400PubMedCrossRef De Renzi E, Cavalleri F, Facchini S (1996) Imitation and utilisation behaviour. J Neurol Neurosurg Psychiatry 61:396–400PubMedCrossRef
9.
go back to reference Wang PN, Miller BL (2007) Clinical aspects of frontotemporal dementia. In: Miller BL, Cummings JL (eds) The human frontal lobes: functions and disorders, 2nd edn. The Guilford Press, New York, pp 279–291 Wang PN, Miller BL (2007) Clinical aspects of frontotemporal dementia. In: Miller BL, Cummings JL (eds) The human frontal lobes: functions and disorders, 2nd edn. The Guilford Press, New York, pp 279–291
10.
go back to reference Piguet O, Hornberger M, Mioshi E, Hodges JR (2011) Behavioural-variant frontotemporal dementia: diagnosis, clinical staging, and management. Lancet Neurol 10:162–172PubMedCrossRef Piguet O, Hornberger M, Mioshi E, Hodges JR (2011) Behavioural-variant frontotemporal dementia: diagnosis, clinical staging, and management. Lancet Neurol 10:162–172PubMedCrossRef
11.
go back to reference Davis PH, Bergeron C, McLachlan DR (1985) Atypical presentation of progressive supranuclear palsy. Ann Neurol 17:337–343PubMedCrossRef Davis PH, Bergeron C, McLachlan DR (1985) Atypical presentation of progressive supranuclear palsy. Ann Neurol 17:337–343PubMedCrossRef
12.
go back to reference Donker Kaat LD, Boon AJW, Kamphorst W, Ravid R, Duivenvoorden HJ et al (2007) Frontal presentation in progressive supranuclear palsy. Neurology 69:723–729PubMedCrossRef Donker Kaat LD, Boon AJW, Kamphorst W, Ravid R, Duivenvoorden HJ et al (2007) Frontal presentation in progressive supranuclear palsy. Neurology 69:723–729PubMedCrossRef
13.
go back to reference Verny M, Duyckaerts C, Agid Y, Hauw JJ (1996) The significance of cortical pathology in progressive supranuclear palsy. Clinico-pathological data in 10 cases. Brain 119:1123–1136PubMedCrossRef Verny M, Duyckaerts C, Agid Y, Hauw JJ (1996) The significance of cortical pathology in progressive supranuclear palsy. Clinico-pathological data in 10 cases. Brain 119:1123–1136PubMedCrossRef
14.
go back to reference Kertesz A, McMonagle P (2010) Behavior and cognition in corticobasal degeneration and progressive supranuclear palsy. J Neurol Sci 289:138–143PubMedCrossRef Kertesz A, McMonagle P (2010) Behavior and cognition in corticobasal degeneration and progressive supranuclear palsy. J Neurol Sci 289:138–143PubMedCrossRef
15.
go back to reference Ghika J, Tennis M, Growdon J, Hoffman E, Johnson K (1995) Environment-driven responses in progressive supranuclear palsy. J Neurol Sci 130:104–111PubMedCrossRef Ghika J, Tennis M, Growdon J, Hoffman E, Johnson K (1995) Environment-driven responses in progressive supranuclear palsy. J Neurol Sci 130:104–111PubMedCrossRef
16.
go back to reference Neary D, Snowden JS, Gustafson L, Passant U, Stuss D et al (1998) Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology 51:1546–1554PubMedCrossRef Neary D, Snowden JS, Gustafson L, Passant U, Stuss D et al (1998) Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology 51:1546–1554PubMedCrossRef
17.
go back to reference Rascovsky K, Hodges JR, Knopman D, Mendez MF, Kramer JH et al (2011) Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain 134:2456–2477PubMedCrossRef Rascovsky K, Hodges JR, Knopman D, Mendez MF, Kramer JH et al (2011) Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain 134:2456–2477PubMedCrossRef
18.
go back to reference Litvan I, Agid Y, Calne D, Campbell G, Dubois B et al (1996) Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele–Richardson–Olszewski syndrome): report of the NINDS-SPSP International Workshop. Neurology 47:1–9PubMedCrossRef Litvan I, Agid Y, Calne D, Campbell G, Dubois B et al (1996) Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele–Richardson–Olszewski syndrome): report of the NINDS-SPSP International Workshop. Neurology 47:1–9PubMedCrossRef
19.
go back to reference De Renzi E, Barbieri C (1992) The incidence of the grasp reflex following hemispheric lesion and its relation to frontal damage. Brain 115:293–313PubMedCrossRef De Renzi E, Barbieri C (1992) The incidence of the grasp reflex following hemispheric lesion and its relation to frontal damage. Brain 115:293–313PubMedCrossRef
20.
go back to reference Dubois B, Slachevski A, Litvan I, Pillon B (2000) The FAB: a frontal assessment battery at bedside. Neurology 55:1621–1626PubMedCrossRef Dubois B, Slachevski A, Litvan I, Pillon B (2000) The FAB: a frontal assessment battery at bedside. Neurology 55:1621–1626PubMedCrossRef
21.
go back to reference Godefroy O, et Groupe de Reflexion pour l’évaluation des Fonctions EXécutives (2008) Fonctions exécutives et pathologies neurologiques et psychiatriques: évaluation en pratique clinique. Solal, Marseille Godefroy O, et Groupe de Reflexion pour l’évaluation des Fonctions EXécutives (2008) Fonctions exécutives et pathologies neurologiques et psychiatriques: évaluation en pratique clinique. Solal, Marseille
22.
go back to reference O Godefroy, P Azouvi, Robert P, Roussel M, LeGall D, on behalf of the Groupe de Réflexion sur l’Evaluation des Fonctions Exécutives Study Group (2010) Dysexecutive syndrome: diagnostic criteria and validation study. Ann Neurol 68:855–864CrossRef O Godefroy, P Azouvi, Robert P, Roussel M, LeGall D, on behalf of the Groupe de Réflexion sur l’Evaluation des Fonctions Exécutives Study Group (2010) Dysexecutive syndrome: diagnostic criteria and validation study. Ann Neurol 68:855–864CrossRef
23.
go back to reference Wechsler D (1981) Wechsler adult intelligence scale-revised manual. Psychological Corporation, New York Wechsler D (1981) Wechsler adult intelligence scale-revised manual. Psychological Corporation, New York
24.
go back to reference Nelson HE (1976) A modified card sorting test sensitive to frontal lobe defects. Cortex 12:313–324PubMedCrossRef Nelson HE (1976) A modified card sorting test sensitive to frontal lobe defects. Cortex 12:313–324PubMedCrossRef
25.
go back to reference Stroop JR (1935) Studies of interference in serial verbal reactions. J Exp Psychol 6:643–661CrossRef Stroop JR (1935) Studies of interference in serial verbal reactions. J Exp Psychol 6:643–661CrossRef
26.
go back to reference Ashburner JT, Friston KJ (2007) Voxel-based Morphometry. In: Friston KJ, Ashburner JT, Kiebel SJ, Nichols TE, Penny WD (eds) Statistical parametric mapping: the analysis of functional brain images. Elsevier: Academic Press, Amsterdam, pp 92–98 Ashburner JT, Friston KJ (2007) Voxel-based Morphometry. In: Friston KJ, Ashburner JT, Kiebel SJ, Nichols TE, Penny WD (eds) Statistical parametric mapping: the analysis of functional brain images. Elsevier: Academic Press, Amsterdam, pp 92–98
27.
go back to reference Mechelli A, Price CJ, Friston KJ, Ashburner J (2005) Voxel-based morphometry of the human brain: methods and applications. Curr Med Imaging Rev 1:1–9CrossRef Mechelli A, Price CJ, Friston KJ, Ashburner J (2005) Voxel-based morphometry of the human brain: methods and applications. Curr Med Imaging Rev 1:1–9CrossRef
28.
go back to reference van Leeuwen ML, van Baaren RB, Martin D, Dijksterhuis A, Bekkering H (2009) Executive functioning and imitation: increasing working memory load facilitates behavioural imitation. Neuropsychologia 47:3265–3270PubMedCrossRef van Leeuwen ML, van Baaren RB, Martin D, Dijksterhuis A, Bekkering H (2009) Executive functioning and imitation: increasing working memory load facilitates behavioural imitation. Neuropsychologia 47:3265–3270PubMedCrossRef
29.
go back to reference Besnard J, Allain P, Aubin G, Chauviré V, Etcharry-Bouyx F et al (2011) A contribution to the study of environmental dependency phenomena: the social hypothesis. Neuropsychologia 49:3279–3294PubMedCrossRef Besnard J, Allain P, Aubin G, Chauviré V, Etcharry-Bouyx F et al (2011) A contribution to the study of environmental dependency phenomena: the social hypothesis. Neuropsychologia 49:3279–3294PubMedCrossRef
30.
go back to reference Brass M, Ruby P, Spengler S (2009) Inhibition of imitative behavior and social cognition. Philos Trans R Soc Lond B Biol Sci 364:2359–2367PubMedCrossRef Brass M, Ruby P, Spengler S (2009) Inhibition of imitative behavior and social cognition. Philos Trans R Soc Lond B Biol Sci 364:2359–2367PubMedCrossRef
31.
go back to reference Brass M, Derrfuss J, von Cramon DY (2005) The inhibition of imitative and overlearned responses: a functional double dissociation. Neuropsychologia 43:89–98PubMedCrossRef Brass M, Derrfuss J, von Cramon DY (2005) The inhibition of imitative and overlearned responses: a functional double dissociation. Neuropsychologia 43:89–98PubMedCrossRef
32.
go back to reference Spengler S, von Cramon DY, Brass M (2009) Control of shared representations relies on key processes involved in mental state attribution. Hum Brain Mapp 30:3704–3718PubMedCrossRef Spengler S, von Cramon DY, Brass M (2009) Control of shared representations relies on key processes involved in mental state attribution. Hum Brain Mapp 30:3704–3718PubMedCrossRef
33.
go back to reference McMurtray AM, Chen AK, Shapira JS, Chow TW, Mishkin F et al (2006) Variations in regional SPECT hypoperfusion and clinical features in frontotemporal dementia. Neurology 66:517–522PubMedCrossRef McMurtray AM, Chen AK, Shapira JS, Chow TW, Mishkin F et al (2006) Variations in regional SPECT hypoperfusion and clinical features in frontotemporal dementia. Neurology 66:517–522PubMedCrossRef
34.
go back to reference Sarazin M, Pillon B, Giannakopoulos P, Rancurel G, Samson Y et al (1998) Clinicometabolic dissociation of cognitive functions and social behavior in frontal lobe lesions. Neurology 51:142–148PubMedCrossRef Sarazin M, Pillon B, Giannakopoulos P, Rancurel G, Samson Y et al (1998) Clinicometabolic dissociation of cognitive functions and social behavior in frontal lobe lesions. Neurology 51:142–148PubMedCrossRef
35.
go back to reference Hashimoto R, Tanaka Y (1998) Contribution of the supplementary motor area and anterior cingulate gyrus to pathological grasping phenomena. Eur Neurol 40:151–158PubMedCrossRef Hashimoto R, Tanaka Y (1998) Contribution of the supplementary motor area and anterior cingulate gyrus to pathological grasping phenomena. Eur Neurol 40:151–158PubMedCrossRef
37.
go back to reference Rizzolatti G, Fabbri-Destro M, Cattaneo L (2009) Mirror neurons and their clinical relevance. Nat Clin Pract Neurol 5:24–34PubMedCrossRef Rizzolatti G, Fabbri-Destro M, Cattaneo L (2009) Mirror neurons and their clinical relevance. Nat Clin Pract Neurol 5:24–34PubMedCrossRef
38.
go back to reference Baier B, Karnath HO (2008) Tight link between our sense of limb ownership and self-awareness of actions. Stroke 39:486–488PubMedCrossRef Baier B, Karnath HO (2008) Tight link between our sense of limb ownership and self-awareness of actions. Stroke 39:486–488PubMedCrossRef
39.
go back to reference Karnath HO, Baier B (2010) Right insula for our sense of limb ownership and self-awareness of actions. Brain Struct Funct 214:411–417PubMedCrossRef Karnath HO, Baier B (2010) Right insula for our sense of limb ownership and self-awareness of actions. Brain Struct Funct 214:411–417PubMedCrossRef
40.
go back to reference Karnath HO, Baier B, Nägele T (2005) Awareness of the functioning of one’s own limbs mediated by the insular cortex. J Neurosci 25:7134–7138PubMedCrossRef Karnath HO, Baier B, Nägele T (2005) Awareness of the functioning of one’s own limbs mediated by the insular cortex. J Neurosci 25:7134–7138PubMedCrossRef
41.
go back to reference Gusnard DA, Akbudak E, Shulman GL, Raichle ME (2001) Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proc Natl Acad Sci USA 98:4259–4264PubMedCrossRef Gusnard DA, Akbudak E, Shulman GL, Raichle ME (2001) Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proc Natl Acad Sci USA 98:4259–4264PubMedCrossRef
42.
go back to reference Northoff G, Bermpohl F (2004) Cortical midline structures and the self. Trends Cogn Sci 8:102–107PubMedCrossRef Northoff G, Bermpohl F (2004) Cortical midline structures and the self. Trends Cogn Sci 8:102–107PubMedCrossRef
43.
go back to reference D’Argembeau A, Ruby P, Collette F, Degueldre C, Balteau E et al (2007) Distinct regions of the medial prefrontal cortex are associated with self-referential processing and perspective taking. J Cogn Neurosci 19:935–944PubMedCrossRef D’Argembeau A, Ruby P, Collette F, Degueldre C, Balteau E et al (2007) Distinct regions of the medial prefrontal cortex are associated with self-referential processing and perspective taking. J Cogn Neurosci 19:935–944PubMedCrossRef
45.
go back to reference Northoff G, Heinzel A, de Greck M, Bermpohl F, Dobrowolny H et al (2006) Self-referential processing in our brain-a meta-analysis of imaging studies on the self. Neuroimage 31:440–457PubMedCrossRef Northoff G, Heinzel A, de Greck M, Bermpohl F, Dobrowolny H et al (2006) Self-referential processing in our brain-a meta-analysis of imaging studies on the self. Neuroimage 31:440–457PubMedCrossRef
46.
go back to reference Cavanna AE, Trimble MR (2006) The Precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583PubMedCrossRef Cavanna AE, Trimble MR (2006) The Precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583PubMedCrossRef
47.
go back to reference Bien N, Roebroeck A, Goebel R, Sack AT (2009) The brain’s intention to imitate: the neurobiology of intentional versus automatic imitation. Cereb Cortex 19:2338–2351PubMedCrossRef Bien N, Roebroeck A, Goebel R, Sack AT (2009) The brain’s intention to imitate: the neurobiology of intentional versus automatic imitation. Cereb Cortex 19:2338–2351PubMedCrossRef
48.
go back to reference Brass M, Zysset S, von Cramon DY (2001) The inhibition of imitative response tendencies. Neuroimage 14:1416–1423PubMedCrossRef Brass M, Zysset S, von Cramon DY (2001) The inhibition of imitative response tendencies. Neuroimage 14:1416–1423PubMedCrossRef
49.
go back to reference Garavan H, Ross TJ, Stein EA (1999) Right hemispheric dominance of inhibitory control: an event-related functional MRI study. Proc Natl Acad Sci USA 96:8301–8306PubMedCrossRef Garavan H, Ross TJ, Stein EA (1999) Right hemispheric dominance of inhibitory control: an event-related functional MRI study. Proc Natl Acad Sci USA 96:8301–8306PubMedCrossRef
50.
go back to reference Uddin LQ, Iacoboni M, Lange C, Keenan JP (2007) The self and social cognition: the role of cortical midline structures and mirror neurons. Trends Cogn Sci 11:153–157PubMedCrossRef Uddin LQ, Iacoboni M, Lange C, Keenan JP (2007) The self and social cognition: the role of cortical midline structures and mirror neurons. Trends Cogn Sci 11:153–157PubMedCrossRef
Metadata
Title
The clinical and anatomical heterogeneity of environmental dependency phenomena
Authors
Julien Lagarde
Romain Valabrègue
Jean-Christophe Corvol
Isabelle Le Ber
Olivier Colliot
Marie Vidailhet
Richard Levy
Publication date
01-09-2013
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 9/2013
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-013-6976-1

Other articles of this Issue 9/2013

Journal of Neurology 9/2013 Go to the issue