Broca's area and temporal organization

I was looking in Neuron to find this paper by Koechlin and Jubault about Broca's area. Here's the abstract:

The prefrontal cortex subserves executive control, i.e., the organization of action or thought in relation to internal goals. This brain region hosts a system of executive processes extending from premotor to the most anterior prefrontal regions that governs the temporal organization of behavior. Little is known, however, about the prefrontal executive system involved in the hierarchical organization of behavior. Here, we show using magnetic resonance imaging in humans that the posterior portion of the prefrontal cortex, including Broca's area and its homolog in the right hemisphere, contains a system of executive processes that control start and end states and the nesting of functional segments that combine in hierarchically organized action plans. Our results indicate that Broca's area and its right homolog process hierarchically structured behaviors regardless of their temporal organization, suggesting a fundamental segregation between prefrontal executive systems involved in the hierarchical and temporal organization of goal-directed behaviors (Koechlin and Jubault 2006:963).

Some definition of exactly what is meant by hierarchical behaviors vs. temporal control and temporal organization is in the first couple of paragraphs:

As revealed by previous studies (Braver et al., 2003, Fuster, 2001 and Koechlin et al., 2003), the temporal dimension of executive control is processed in the lateral prefrontal cortex by a top-down control system of executive processes extending from premotor to the most anterior prefrontal regions. In this system, more anterior regions integrate temporally more dispersed information for selecting appropriate behaviors at each time. This prefrontal system, however, is not involved in the precise timing of motor acts underlying the execution of motor sequences, a distinct function associated with medial regions of the premotor cortex including the supplementary motor area complex (Kennerley et al., 2004 and Tanji, 2001).

It seems plausible to me that these systems are involved in learning the steps of temporally organized processes that later become more-or-less automatic, as sequences are slowly accommodated by executive (i.e., conscious) control and then are established by repeated use into rapid motor sequences. So how does "hierarchical organization" differ from this sequential organization?

Another basic dimension of executive control is the hierarchical organization of behavior. In this dimension, appropriate actions are selected as subordinate elements that compose ongoing structured action plans rather than from occurrences of temporally distant events. In other words, action selection may result from processing the hierarchical structure of action plans evoked by external events rather than processing crosstemporal contingencies between events. Little is known about the prefrontal executive system subserving action selection based on hierarchical structures of behavioral plans.

In other words, not just what to do at which time, but what to do in relation to other actions, all organized in time. At one level, these hierarchical plans may include discrete or automatic motor sequences in combination with executive direction on the basis of external events, and in ways responsive to different, possible distant, parts of the action sequence.

These kinds of hierarchical behaviors are necessary for language, since meaning depends on grammatical relations, which are themselves hierarchical rules for encoding relational information in a temporal sequence. So, the authors hypothesized that Broca's area, necessary for grammar, might also be necessary for these kinds of temporal plans.

And they discovered that they were right:

[A]nterior BCA regions show phasic activation at boundaries of superordinate chunks only, providing evidence that these regions are specifically involved in selecting or inhibiting superordinate action chunks. Compared to anterior BCA regions, posterior BCA regions additionally exhibited phasic activations at boundaries of simple chunks and in the transitions between simple chunks forming superordinate actions. Thus, posterior BCA regions are involved in selecting and inhibiting simple action chunks in response to external signals or as successive components of ongoing superordinate actions. Posterior BCA regions also showed phasic activation at boundaries of superordinate chunks. As explained above, such activations are unlikely to result from externally guided, bottom-up selection/inhibition of simple chunks in response to start and stop cues. Instead, such activations provide evidence that top-down control is exerted from anterior to posterior BCA regions and conveys trigger signals for starting and stopping successive selection of component simple chunks at the boundaries of superordinate chunks. Premotor regions showed the same activation profile as posterior BCA regions except that they showed additional phasic activations in transitions between motor responses composing simple action chunks (Figure 4). Reasoning as above, we conclude that premotor regions are involved in selecting motor acts in response to stimuli or as successive components of ongoing simple action chunks. Top-down control is exerted from posterior BCA to premotor regions for starting and stopping successive selection of component motor acts at the boundaries of simple chunks.

The whole prefrontal cortex seems to be involved in a series of finer and finer temporal planning and processing from anterior to posterior. Broca's area, and the posterior part of it referenced here, are relatively far back in this series of areas, and are involved with starting and stopping sequences that are carried out by the next area back, the premotor cortex. Toward the front, more general temporal planning occurs, along with the activation of entire hierarchical sequences in response to external events.

This front-to-back organization appears to hold within Broca's area itself, with respect to language processing:

Clearly, these accounts of the role of Broca's area in language appear compatible with the system of hierarchical control we propose. Language studies also reveal that in Broca's area posterior regions (i.e., BA 44/BA6) are preferentially engaged in language tasks based on phonological processing, whereas anterior regions (i.e., BA 45/BA 44) and anterior-ventral regions (i.e., BA 47/BA 45) are more specifically involved in tasks based on syntactic and semantic processing, respectively (review in Bookheimer [2002]; e.g., Gough et al., 2005). Given that syntactic and semantic processing involve hierarchically higher linguistic representations (i.e., words and multiword utterances) than those involved in phonological processing (phonemes/syllables within words), such functional segregation in the language domain appears consistent with our findings indicating an anterior-posterior organization of Broca's area in hierarchical control. Thus, our results support the view that Broca's area implements an executive function specialized for processing hierarchical structures in multiple domains of human cognition (Thompson-Schill et al., 2005). We speculate that the modular executive system of hierarchical control we describe possibly captures key functional components that may explain the critical contribution of Broca's area to human language.

It was interesting to me that I was just thinking and writing a bit about this topic yesterday. A longstanding issue has been whether grammar was itself an adaptation that followed (or coincided with) the evolution of language, or whether basic grammatical abilities might have evolved earlier for some other purpose, later exapted for use in language. The latter position has been at times advocated by Stephen J. Gould and Noam Chomsky.

This study would seem to make clear that grammatical aspects of language are lodged in our left Broca's area precisely because they require the kinds of temporal hierarchical organization that this region of cortex already carried out in earlier primates. This seems a bit distant from some suggestions about the prelinguistic function of grammar -- for instance, that it may have functioned as some kind of "language of thought". But at the same time it raises the possibility that other nonlinguistic but temporally hierarchical actions in early hominids may have biased them toward greater abilities in this area -- for example, tool production and associated action sequences.

Anyway, these are not new thoughts. I think the important thing is the emergence through these studies of a kind of simplicity in the organization of the prefrontal cortex, at least with respect to planning and carrying out time-related activities. It may be an interesting developmental analogue to other areas of the cortex, such as the sensory and motor cortices (each consisting of a homuncular map of the body) and the visual cortex (which includes a map of the visual field).

References:

Koechlin E, Jubault T. 2006. Broca's area and the hierarchical organization of human behavior. Neuron 50:963-974.DOI link