Tuesday, August 24, 2010

Neuroimaging of language: Why hasn't a clearer picture emerged?

This is the question raised in a paper by Evelina Fedorenko and Nancy Kanwisher published last year in Language and Linguistics Compass. The main point that they want to make is that language neuroimagers need to stop doing group studies and start doing functional localization in individual subjects, like the vision folks do. I don't disagree at all; e.g., see this post. In fact, we have used individual subject analyses in several of our papers (e.g., Okada & Hickok, 2006; Okada et al., in press).

What I found a bit on the irritating side though was the extremely dim and distressingly myopic view of progress in the field of the neural basis of language. They start by stating that two questions have

driven dozens of studies on the neural basis of language published in the last several decades: (i) Are distinct cortical regions engaged in different aspects of language? (ii) Are regions engaged in language processing specific to the domain of language?

And they suggest that "Neuroimaging has not yet provided clear answers to either question".

Regarding question one, there is strong evidence from functional imaging regarding the involvement of distinct cortical regions/circuits in phonemic (STS), lexical-semantic (MTG), prosodic (anterior dorsal STG), and higher-level combinatorial processes (anterior temporal/inferior frontal regions). Additional circuits have been delineated that support auditory-motor integration and auditory/phonological short-term memory. Here are some relevant reviews of this literature: Binder et al., 2000; Hickok and Poeppel, 2007; Indefrey and Levelt, 2004.

Regarding question two, several studies have clearly identified voice-specific responses in the STG (Belin et al. 2000), higher-level speech specific responses in the STS (Scott et al. 2000; Okada et al. 2010), and even what we might as well call the anterior temporal lobe sentence area, given how selective it is to the perception of sentence-level stimulation (Humphries et al., 2006; Humphries et al., 2005; Humphries et al., 2001; Rogalsky and Hickok, 2009; Vandenberghe et al., 2002). But more importantly, some of us have moved beyond the specificity issue with the aim of trying to identify the circuits and computations involved in a given process whether or not it is special to speech.

So F&K are a bit misinformed in regarding the contribution of neuroimaging to the questions they raise.

Even worse, though, is their summary of "where things stand" concerning our understanding of the "neural basis of language" -- a rather sweeping domain, especially if they have in mind only the two questions they raise at the outset. Nonetheless, concerning the Neural Basis of Language they emphasize:

1. that the 19th century idea that Broca's area = speech production and Wernicke's area = speech comprehension doesn't hold up to modern data

2. that left frontal regions activate to a variety of language tasks, and indeed even non-linguistic tasks

3. that regions outside of the traditional peri-Sylvian cortex activate during language processing

4. that meta analyses show lots of overlap between language tasks

This is frankly a pathetic summary of the state of the field and a pretentious starting point for the methodological schooling that F&K provide in the following sections of their paper.

Completely ignored in this summary is (i) a body of work showing that much of the confusion (and overlapping activations) evaporates if one is careful about task selection (Hickok & Poeppel, 2007), (ii) convergence on the involvement of the STS in phonemic level processes in speech perception (Leibenthal et al., 2005; Scott & Johnsrude, 2003; Hickok & Poeppel, 2007), (iii) convergence on the idea of a dual stream architecture in language system (Hickok & Poeppel, 2007; Rauchecker & Scott, 2009), (iv) recent progress in mapping the circuit that supports sensory-motor integration in speech processing (Golfinopoulus et al. 2009; Hickok et al., 2009), (v) progress in understanding the basis of hemispheric asymmetries for acoustic and phonemic processing in auditory cortex (Boemio, et al. 2005); Zatorre, et al. 2002) , (vi) convergence on the idea that anterior temporal regions support some aspect of sentence-level processing (the linguistic equivalent of the FFA), (vii) convergence on the relation between sensory-motor circuits and phonological short-term memory (Buchsbaum et al. 2008; Postle, 2006)... I could go on.

Yes, there is still plenty of murkiness, much of it surrounding the function of Broca's area, and yes, individual subject analyses would be helpful, but it is not a magic bullet (e.g., task selection is more important in my view) -- e.g., I'm willing to bet that the vision folks still have some work to do -- and the existence of murkiness doesn't justify the characterization of an entire field as failing to make progress due to methodological ineptness. This kind of argumentation was prominent in another of Fedorencko's papers that was featured prominently on this blog. It's a bit disturbing to see it showing up again.

F&K's paper has generated a more formal (i.e., published) response by Grodzinsky (2010) who is critical of their take on the field as well but for different reasons. Definitely worth a look.

The field of the neural basis of language has made significant progress in the last several years, despite what F&K assert.


Fedorenko, E., & Kanwisher, N. (2009). Neuroimaging of Language: Why Hasn't a Clearer Picture Emerged? Language and Linguistics Compass, 3 (4), 839-865 DOI: 10.1111/j.1749-818X.2009.00143.x

Binder, J.R., Frost, J.A., Hammeke, T.A., Bellgowan, P.S., Springer, J.A., Kaufman, J.N., and Possing, E.T. (2000). Human temporal lobe activation by speech and nonspeech sounds. Cerebral Cortex 10, 512-528.

Belin, P., Zatorre, R.J., Lafaille, P., Ahad, P., and Pike, B. (2000). Voice-selective areas in human auditory cortex. Nature 403, 309-312.

Buchsbaum, B.R., and D'Esposito, M. (2008). The search for the phonological store: from loop to convolution. J Cogn Neurosci 20, 762-778.

Golfinopoulos, E., Tourville, J.A., and Guenther, F.H. (2009). The integration of large-scale neural network modeling and functional brain imaging in speech motor control. Neuroimage.

Grodzinsky, Yosef. 2010. A clearer view of the linguistic brain: reply to Fedorenko and Kanwisher. Language and Linguistic Compass, 4, pp. 605-622.

Hickok, G., and Poeppel, D. (2007). The cortical organization of speech processing. Nat Rev Neurosci 8, 393-402.

Humphries, C., Binder, J.R., Medler, D.A., and Liebenthal, E. (2006). Syntactic and semantic modulation of neural activity during auditory sentence comprehension. J Cogn Neurosci 18, 665-679.

Humphries, C., Love, T., Swinney, D., and Hickok, G. (2005). Response of anterior temporal cortex to syntactic and prosodic manipulations during sentence processing. Human Brain Mapping 26, 128-138.

Humphries, C., Willard, K., Buchsbaum, B., and Hickok, G. (2001). Role of anterior temporal cortex in auditory sentence comprehension: An fMRI study. Neuroreport 12, 1749-1752.

Indefrey, P., and Levelt, W.J. (2004). The spatial and temporal signatures of word production components. Cognition 92, 101-144.

Liebenthal, E., Binder, J.R., Spitzer, S.M., Possing, E.T., and Medler, D.A. (2005). Neural substrates of phonemic perception. Cereb Cortex 15, 1621-1631.

Okada, K., and Hickok, G. (2006). Identification of lexical-phonological networks in the superior temporal sulcus using fMRI. Neuroreport 17, 1293-1296.

Okada, K., Rong, F., Venezia, J., Matchin, W., Hsieh, I.H., Saberi, K., Serences, J.T., and Hickok, G. (in press). Hierarchical Organization of Human Auditory Cortex: Evidence from Acoustic Invariance in the Response to Intelligible Speech. Cereb Cortex.

Postle, B.R. (2006). Working memory as an emergent property of the mind and brain. Neuroscience 139, 23-38.

Rauschecker, J.P., and Scott, S.K. (2009). Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat Neurosci 12, 718-724.

Rogalsky, C., and Hickok, G. (2009). Selective Attention to Semantic and Syntactic Features Modulates Sentence Processing Networks in Anterior Temporal Cortex. Cereb Cortex 19, 786-796.

Scott, S.K., and Johnsrude, I.S. (2003). The neuroanatomical and functional organization of speech perception. Trends Neurosci 26, 100-107.

Scott, S.K., Blank, C.C., Rosen, S., and Wise, R.J.S. (2000). Identification of a pathway for intelligible speech in the left temporal lobe. Brain 123, 2400-2406.

Vandenberghe, R., Nobre, A.C., and Price, C.J. (2002). The response of left temporal cortex to sentences. J Cogn Neurosci 14, 550-560.


David Poeppel said...

I am a grumpy middle-aged guy, and I tend to be pretty critical of basically everything I come across -- but even I am not as negative about the state of the field as Fedorenko and Kanwisher ... I think they seriously underestimate the sophistication of some of the current work, and Greg has already pointed out that there is a literature dealing with their specific complaints.

Let me amplify one point. While functional imaging -- and as a consequence functional localization -- plays a dominant role in the field, a lot of research effort is going into increasingly detailed analyses of the tasks, and specifically the computational subroutines underlying the execution of the experimental tasks.

We are presumably all pulling in the same direction, aiming for theoretically well motivated, computationally explicit, and neurobiologically solidly grounded accounts of speech and language, so I would welcome new approaches to understand things more deeply -- but the suggestions articulated by F&K are not yet mature enough to motivate me to adopt that perspective, given the tangible progress we have already made.

Whitney Anne Postman said...

Can I get a shout-out for neuro-imaging lesion studies, e.g., Myrna Schwartz et al's masterpiece in "Brain" last year? http://www.talkingbrains.org/2009/12/role-of-anterior-temporal-lobe-in.html
If work like this is not considered to contribute to a clearer picture of the neural basis of language, then I gotta develop an Academic Optimism pill.

Anonymous said...

For a response from Fedorenko & Kanwisher and additional discussion, see http://www.talkingbrains.org/2010/08/response-from-fedorenko-kanwisher.html