Value = 0.001%

4

3

2

1

0

-1

W B B W B W P P

4

3

2

1

0

-1

Relating imaging and patient studies of tool processingJ. Devlin1,2, C. Moore1, C. Mummery1, J. Phillips1, M. Gorno-Tempini1, M. Rushworth1,2, and C. Price1

1Wellcome Department of Cognitive Neurology, Institute of Neurology2Centre for Functional Magnetic Resonance Imaging of the Brain, University of Oxford

Study Categories Stimuli Task

1. Mummery et al (1996) A, T Spoken words Category fluency

2. Mummery et al (1998) A, T Written words Semantic & syllable

decisions

3. Moore & Price (1999) A, F, T, V Pictures Naming

4. Moore & Price (1999) A, F, T, V Written words Matching

and pictures

5. Gorno-Tempini (2000) Fa, A, T Pictures Naming

6. Phillips et al (submitted) F, T Written words Semantic & screen

and pictures size decisions

Abbreviations: A=animals, F=fruit, Fa=famous faces, T=tools, V=vehicles.

Several functional neuroimaging studies have reported a region in the left posterior middle temporal cortex that is more active when words and pictures represent tools than other categories of objects (see Fig. 1 and ref. 14 for a review). This area is not damaged, however, by fronto-parietal lesions typically associated with selective deficits for man-made items4. The lesion data is more consistent with the few imaging studies that have reported increased left pre-motor activation for tools2, 7, 9.

Background

Activation in the left posterior middle temporal cortex (LPMT) and left pre-motor area in normals in a picture naming task from (Martin et al. 1996)

Figure 1: Tools activate LPMT

The current study investigated tool-associated brain activations in an attempt to reconcile the apparent discrepancies between the imaging and lesion literature.

Data from 50 subjects performing 6 experiments were acquired on a single PET scanner (see Table)

Single multi-factorial analysis with three factors:

1) Category (natural vs. man-made)

2) Task

3) Stimulus type

Man-made items divided in tools and non-tools.

Current Study

Table

L

Figure 2: Tools > Living thingsfor semantic tasks only

L. ventral pre-motor(-42, 4, 18)

SPM{Z}=3.6p<0.001 uncorrected

L. posterior middletemporal cortex

(-62, -58, 0)SPM{Z}=5.3

p<0.005 corrected

L. anterior supramarginal(-60, -24, 34)SPM{Z}=3.8

p<0.001 uncorrected

Figure 3: Effect sizes for tools

%rC

BF

ch

ang e

1. L. post. Middle temproal gyrus

2. L. ventral pre-motor area

%rC

BF

ch

ang e

W B B W B W P P

Contrasts1. Syllable decisions12

2. Screen size decisions13

3. Semantic decisions13

4. Semantic decisions12

5. W-P matching10

6. Category fluency11

7. Naming pictures6

8. Naming pictures10

3. L. anterior supramarginal gyrus

Phonological tasks W WordsPerceptual tasks P PicturesSemantic decision tasks B Both words andWord retrieval tasks pictures

Key

Tasks without a strong semantic component (e.g. screen size decisions and syllable decisions) did not show a consistent advantage for tools

More semantic tasks, on the other hand, such as semantic decisions and picture naming, revealed small ( <3% rCBF changes) but consistent effects for tools > living things

W B B W B W P P

4

3

2

1

0

-1

First study to demonstrate LPMT activation for tools relative to living things at a corrected level of significance. May be due to:

Small effect sizes (<3% rCBF) and Context-specific effects, i.e. category effects were

only present in tasks required semantic processing

Results consistent with previous imaging studies showing Tools > Animals in ventral pre-motor cortex BUT also demonstrated that this effect was not present relative to fruit

No area was activated only by tools

Summary of results

Tools relative to living things activated three regions in the left hemisphere (see Fig. 2):

1. Posterior middle temporal cortex (LPMT)

2. Ventral pre-motor cortex

3. Anterior supramarginal gyrus

but only for tasks with a strong semantic component (see Fig. 3)

Results

Results (cont.)

References

1. Binkofski et al. (1998). Human anterior intraparietal areas subserves prehension: a combined lesion and fMRI activation study. Neurology, 50, 1253-1259.

2. Chao, L. L., & Martin, A. (2000). Representation of manipulable man-made objects in the dorsal stream. NeuroImage, 12, 478-484.

3. Ehrsson et al. (2000) Cortical activity in precision- versus power-grip tasks: An fMRI study. J. Neurophysiology, 83, 528-536.

4. Gainotti, G. (2000). What the locus of brain lesion tells us about the nature of the cognitive deficit underlying category-specific disorders: a review. Cortex, 36, 539-559.

5. Gallese, V., & Goldman, A. (1998). Mirror neurons and the simulation theory of mind-reading. Trends in Cognitive Science, 2(12), 493-501.

6. Gorno-tempini, M. L., Cipolotti, L., & Price, C. J. (2000). Which level of object processing generates category specific differences in brain activation? Proceedings of the Royal Society, London B, 1253-1258.

7. Grabowski, T. J., Damasio, H., & Damasio, A. R. (1998). Premotor and prefrontal correlates of category-related lexical retrieval. NeuroImage, 7, 232-243.

8. Jeannerod, M., Arbib, M. A., Rizzolatti, G., & Sakata, H. (1995). Grasping objects: the cortical mechanisms of visuomotor transformation. Trends in Neuroscience, 18(7), 314-320.

9. Martin, A., Wiggs, C., Ungerleider, L., & Haxby, J. (1996). Neural correlates of category-specific knowledge. Nature, 379, 649-652.

10. Moore, C. J., & Price, C. J. (1999). A functional neuroimaging study of the variables that generate category specific object processing differences. Brain, 122, 943-962.

11. Mummery, C. J., Patterson, K., Hodges, J., & Wise, R. J. (1996). Generating 'tiger' as an animal name or a word beginning with T: Differences in brain activation. Proceedings of the Royal Society of London B Biological Sciences, 263, 989-995.

12. Mummery, C. J., Patterson, K., Hodges, J. R., & Price, C. J. (1998). Functional neuroanatomy of the semantic system: Divisible by what? Journal of Cognitive Neuroscience, 10(6), 766-777.

13. Phillips, J., Noppeney, U., Humphreys, G. W., & Price, C. J. (submitted). A positron emission tomography study of action and category.

14. Price, C. J. & Friston, K. J. (in press) What has neuroimaging contributed to category-specificity? In G. Humphreys & E. Forde (Eds.), Category specificity in mind and brain . Sussex, England: Psychology Press.

Discussion These findings correspond well with the

neurophysiological literature showing that in monkeys neurons in the ventral pre-motor area F5 respond to visually presented graspable objects such as tools and fruit5, 8.

This region is part of a “visuo-action” network including pre-motor (F5), anterior intra-parietal (AIP/7b), and inferior bank of the superior temporal sulcus (STS) regions (see Fig. 4)

F5

AIP

7b

STS

Adopted from Jeannerod et al. (1995)

Figure 4: Macaque “visuo-action” network

The three regions identified in the current study may be homologues of this visuo-action network.

The same regions often activated in human imaging studies of grasping or hand movements1,3

These results provide a plausible explanation for patients with semantic impairments to man-made items who typically have large left fronto-parietal lesions:

Although the LPMT is spared, the lesion can affect the inferior parietal and ventral pre-motor regions and the connections between them.

Q: Were these activations truly category-specific?

Relative effect sizes

A Fr V T FF A Fr V T MN SN

Word-picture matching10

Picture naming10

A Fr V T FF A Fr V T

KeyA Animals Fr Fruit BP Body parts T ToolsFa Famous Faces V VehiclesFF False fonts

1. L. posterior middle temporal area?

2. L. ventral pre-motor area?

3. L. anterior supramarginal area?

Fa A T BP

Picture naming6

Tools (T), simple non-objects (SN) and body parts (BP)all activated the LPMT.

Relative effect sizes

Word-picture matching10

Picture naming10

Fruit (Fr) and tools (T) both activate the ventral pre-motor region.

Relative effect sizes

Word-picture matching10

Picture naming10

A Fr V T FF A Fr V T

Tools (T) and false fonts (FF) activated the anteriorsupramarginal region.

L R L R L R

1 2 3 4 5 6 7 81 2 3 4 5 6 7 8

1 2 3 4 5 6 7 8

KeyA Animals FF False fontsFr Fruit T ToolsV Vehicles

KeyA Animals FF False fontsFr Fruit T ToolsV Vehicles