ios press induction of semantic impairments using rtms...

Behavioural Neurology 23 (2010) 217–219 217DOI 10.3233/BEN-2010-0299IOS Press

Induction of semantic impairments usingrTMS: Evidence for the hub-and-spokesemantic theory

Gorana Pobrica,∗, Elizabeth Jefferiesb and Matthew A. Lambon RalphaaNeuroscience and Aphasia Research Unit, School of Psychological Sciences, University of Manchester,Manchester, UKbDepartment of Psychology, University of York and York Neuroimaging Centre, York, UK

1. Introduction

Semantic cognition permits us to bring meaning toour verbal and nonverbal experiences and to generatecontext-and time-appropriatebehaviour [1,2]. It is coreto language and nonverbal skilled behaviours (e.g., us-ing objects), and when impaired after brain damage,it generates significant disability [3]. A fundamen-tal neuroscience question, therefore, is how does thebrain code and generate semantic cognition? Historicaland some contemporary theories emphasise that con-ceptualisation stems from the joint-action of modality-specific association cortices (the “distributed” theo-ry) [4,5] reflecting our accumulated verbal, motor andsensory experiences. Parallel studies of semantic de-mentia, rTMS in normal participants and neuroimag-ing indicate that the anterior temporal lobe (ATL) playsa crucial and necessary role in conceptualisation bymerging experience into an amodal semantic represen-tation [1,2,6–8].

To date, studies have focussed on the contribution ofeither modality-specific association regions or the ATLto semantic memory. In this rTMS investigation, wetested the differential contribution of both regions forthe first time. Like neuropsychological studies, rTMS

∗Corresponding author: Dr. Gorana Pobric, Neuroscience andAphasia Research Unit (NARU), School of Psychological Sci-ences (Zochonis Building), University of Manchester, Oxford Road,Manchester, M13 9PL UK. Tel.: +44 161 275 1967; Fax: +44 161275 2873; E-mail: [email protected].

can be used to test the necessity of regions for cognitivefunction. It has the additional, unique benefit that thefunctional contribution of multiple regions can be suc-cessively compared within the same participants. Weused this approach to delineate between three differenthypotheses: (a)distributed-only– concepts reflect theconjoint action of modality-specific areas alone withoutthe ATL; (b) hub-only– in which concepts are formedwithin the ATL and modality-specific regions only pro-vide sensorimotor input/output gateways rather thanmaking a necessary contribution to conceptualisation;(c)hub-and-spoke– in which modality-specific regionsprovide the basic sensory, motor and verbal ingredi-ents whilst the ATL hub supports an additional amodalrepresentation which codes the pan-modal, deep statis-tical structure and thus generates a high-dimensional,modality-independent similarity matrix [1,8]. Underthis latter account, both the ATL “hub” and modality-specific “spokes” provide necessary and important con-tributions to conceptualisation.

We adjudicated between these competing theories byinvestigating category-specific impairments. To date,these have only ever been observed clinically; somepatients present with relatively greater problems forone domain than another (e.g., poorer performance foranimals than manmade items) [9,10]. The feature-weighting hypothesis [9] proposes that categories arereliant on different sources of information, coded bymodality-specific regions. This provides a methodfor testing the different theories of conceptualisation.Specifically, we compared the effect of stimulating the

ISSN 0953-4180/10/$27.50 2010 – IOS Press and the authors. All rights reserved

218 G. Pobric et al. / Induction of semantic impairments using rTMS

Fig. 1. The effect of rTMS stimulation on naming.

ATL and IPL in normal participants (by applying rTMSoff-line for 10 min at 1-Hz (600 s at 120% motor thresh-old level) over left ATL (−53, 4,−32), left IPL (−49,−44, 48) and occipital pole (Oz) prior to naming pic-tures and number. If the ATL is involved in seman-tic memory, as proposed, then rTMS should generatea category-general effect. If the IPL spoke is impli-cated then stimulation should impact on semantic per-formance but only for concepts that rely on praxis in-formation – i.e., manipulable manmade objects. Thusstimulation at this site should induce a category-specificimpairment which, as far as we are aware, has neverbeen demonstrated before in neurologically-intact par-ticipants.

ATL stimulation generated a selective slowing of ba-sic level naming [t(8)= −3.3, p < 0.05] but had noimpact on number naming, adding to previous evidencefor the involvement of the ATL in semantic process-ing [6]. Stimulation of the occipital control site had noimpact on either task, indicating no generalised, non-specific effect of rTMS (see Fig. 1a).

To examine emerging category effects from original200 items we created two lists of living and non-livingitems matched for familiarity, frequency and visualcomplexity. Each stimulation site produced significant-

ly different effects on the two categories. There wasa category-general effect for ATL stimulation [namingtimes slowed for living t(8)= 2.391,p < 0.05] andnonliving items [t(8)= 2.394,p < 0.05]. In contrast,left IPL stimulation only slowed responses for nonliv-ing items [t(8)= 3.1, p < 0.05]. Again there wasno effect after rTMS to the occipital control site (seeFig. 1b).

To confirm that the IPL category effect reflectedthe coding of praxis information, we compared the ef-fect of rTMS to two matched sets of manipulable vs.non-manipulable manmade items. The same patternemerged across the three sites: ATL stimulation slowedboth sets of manmade items [low manipulable (t(8)= 2.34, p < 0.05) and high manipulable items (t(8)= 2.31, p < 0.05)]. Crucially, left IPL stimulationslowed responses for high manipulable items only [t(8)= −4.21,p < 0.05]. In addition, TMS delivered tothe occipital control site had no significant effects onnaming times (see Fig. 1c).

In summary, through the use of rTMS in normalparticipants, we have been able to demonstrate twocontrasting effects. Stimulation of the ATL leads toa generalised slowing of semantic processing acrossall types of concept (living, manipulable objects and

G. Pobric et al. / Induction of semantic impairments using rTMS 219

non-manipulable items). This is in keeping with thecategory-general effects observed in semantic demen-tia [1–3]. In contrast, stimulation to the IPL generatesa category-specific pattern reflective of the praxis in-formation coded in this neural region. As far as weare aware, this is the first time that a category-specificdeficit has been generated in normal participants.

In conclusion, the findings of this study fit squarelywith thehub-and-spokemodel of semantic memoryandrule out the other models. Both the ATL amodal huband the modality-specific association “spokes” con-tribute to semantic representations. Because the ATLhub is involved in the translation and deeper encodingof pan-modal information sources, the representationsbecome modality-invariant [1,2,9] and thus they are in-volved in conceptualisation for all types of category.In contrast, modality-specific sources of informationonly contribute to the subset of concepts that are expe-rienced in that modality. Unlike of modality-specificareas, IPL is an ideal test-bed for this given that there isan almost binary division of praxis experience betweenmanipulable objects and other concepts.

Acknowledgements

The study was supported by an RCUK fellowship, aWellcome project grant (078734/Z/05/Z) and an MRCprogramme grant (G0501632).

References

[1] M.A. Lambon Ralph and K. Patterson,Ann NY Acad Sci1124(2008), 61–76.

[2] K. Patterson, P.J. Nestor and T.T. Rogers,Nat Rev Neurosci8(2007), 976–987.

[3] J.R. Hodges, K. Patterson, S. Oxbury and E. Funnell,Brain115 (1992), 1783–1806.

[4] G.H. Eggert,Mouton, The Hague (1977).[5] A. Martin, Annu Rev Psychol58 (2007), 25–45.[6] G.G. Pobric, E. Jefferies and M.A. Lambon Ralph,PNAS104

(2007), 20137–20141.[7] J.R. Binder, R.H. Desai, W.W. Graves and L.L. Conant,Cereb

Cortex, (2009).[8] T.T. Rogers et al.Psychol Rev111 (2004), 205–235.[9] E.K. Warrington and T. Shallice,Brain 107 (1984), 829–854.

[10] B.Z. Mahon and A. Caramazza,Annu Rev Psychol60 (2009),27–51.

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