Research Briefing: Dynamic population coding for flexible cognition

Dynamic population coding in prefrontal cortex

Our environment is in constant flux. At any given moment there could be a shift in scenario that demands an equally rapid shift in how we interpret the world around us. For example, the meaning of a simple traffic light critically depends on whether you are driving to work or travelling on foot. Our brains must constantly adapt to accommodate an enormous range of such possible scenarios - in this study, we applied new analysis tools to explore how patterns of brain activity change for different task contexts, allowing for flexible cognitive processing (in Stokes et al., 2013, Neuron; see also Comment by Miller and Fusi in the same issue).

Prefontal Cortex

Adapted from Fig 1

We focused our investigation on an area in the frontal lobe known as lateral prefrontal cortex. This brain area has long been implicated in flexible cognitive processing. Damage to prefrontal cortex is classically associated with reduced cognitive flexibility (Luria, 1966) as part of a more general dysexecutive syndrome. In studies using functional magnetic resonance imaging (fMRI), lateral frontal cortex is also usually more active when participants perform tasks that demand cognitive flexibility (Wager et al., 2004). It it widely believed that prefrontal cortex is especially important for representing information about our environment and task goals in mind for guiding flexible behaviour (Baddeley, 2003; Miller, 2000).

Dynamic coding population coding

Dynamic trajectory through state-space

In this study, we observe a highly dynamic process underlying flexible cognitive processing using a statistical approach that allows us to decode the patterns of population-level activity in prefrontal cortex at high temporal resolution. During a task that requires a different stimulus-response mapping according to trial-by-trial instruction cues (see Fig 1), we found that the pattern of activity rapidly changes during processing of the instructive cue stimulus. After this complex cascade through activity state-space (for more info, see Stokes, 2011), overall activity levels return to baseline for the remainder of a delay period spanning the instruction cue and a possible target stimulus.

Adapted from Fig 5

However, the effect of the cue response lingers on. Subsequent stimuli elicit a population response that critically depends on the previous cue identity. In other words, the dynamic population response triggered by the cue stimulus shifts the response profile of the network of prefrontal cells. This shift in tuning profile allows us to decode the current task-rule (i.e., cue indentify) based on a simple driving stimulus (i.e., neutral stimuli, see Fig 5).

Adapted from Fig 6

More importantly, the shift in the network response profile could also underlie task-dependent target processing (i.e., choice stimuli, see Fig 6). The population response to potential target stimuli rapidly evolved from a stimulus-specific coding scheme, to a more abstract code that distinguishes only between different target and non-target items. This dynamic tuning property is ideal for flexible cognition (Duncan, 2001).

Putative mechanism: flexible connectivity

The flow of brain activity critically depends on the pattern of connections between neurons. Contrary to intuition, these connections are always changing. The pattern of connections that make up the very essence of personal experience is constantly adjusting and adapting to the myriad changes experienced throughout life.

Synaptic Plasticity [wiki commons]

Extensive research focuses on long-term structural changes in connectivity through synaptic plasticity, however the rapid changes we experience from moment-to-moment requires a more flexible kind of memory that can represent the transient features of a given scenario. This kind of flexible "online" memory is typically referred to as ‘working memory’.

It has long been assumed that working memory is maintained by keeping a specific thought in mind, like a static snapshot of a visual image or an abstract goal such as ‘turn left at the next set of lights’. However, more recent evidence suggests that working memory can also be stored by laying down specific, but temporary neural pathways (e.g., Mongillo, Barak & Tsodyks, 2008). Neural pathways are formed by synaptic connections. In a comprehensive review of the literature on short-term synaptic plasticity, Zucker (1989) writes: “Chemical synapses are not static. Postsynaptic potentials wax and wane, depending on the recent history of presynaptic activity”. Short-term plasticity could provide a key mechanisms for flexible connectivity that is necessary for rapid, but temporary changes in network behaviour.

This new idea allows for a more dynamic theory of brain function, which is more consistent with the everyday experience of continuous thought processes that seem to evolve through time, rather than persist as a static representation. We suggest that short-term plasticity could help explain our data:

Adapted from Fig 7

The initial instruction cue stimulus establishes a specific (but temporary) connectivity state during the most active phase of the response. This would explain why the pattern constantly changes - if the synapse are constantly changing, then even identical input to the system will result in constantly shifting output patterns (Buonomano and Maass, 2009). This temporary shift in the response sensitivity of the prefrontal network allows the identity of previous input to be decoded by the patterned response to subsequent input, consistent with the silent memory hypothesis. Finally, dynamic changes in connectivity could also be used to rapidly shift the tuning profile of the prefrontal network to accommodate changes in what specific stimuli mean for behaviour (see Fig. 7).

Broader implications

Brain activity is inherently non-stationary - the continuity/stability of cognitive states are unlikely to depend on static activity states, but rather rapid changes in temporary connectivity patterns. This research also raises the intriguing possibility that cognitive capacity limits are not so much constrained by the sheer amount of information that we can keep in mind, but rather how we can put that information to use. Further research in our lab will explore these exciting possibilities.


Reference:

Stokes, Kusunoki, Sigala, Nili, Gaffan and Duncan (2013). Dynamic Coding for Cognitive Control in Prefrontal Cortex. Neuron, 78, 364-375 [here]

Also see coverage: Miller Lab (MIT), Neuron Preview


Other literature cited:

Baddeley, A. (2003). Working memory: looking back and looking forward. Nat. Rev. Neurosci. 4, 829–839. [here]

Buonomano, D.V., and Maass, W. (2009). State-dependent computations: spatiotemporal processing in cortical networks. Nat. Rev. Neurosci. 10, 113–125. [here]

Luria, A.R. (1966). Higher Cortical Functions in Man (New York: Basic Books).

Miller, E.K. (2000). The prefrontal cortex and cognitive control. Nat. Rev. Neurosci. 1, 59–65. [here]

Mongillo, G., Barak, O., and Tsodyks, M. (2008). Synaptic theory of working memory. Science 319, 1543–1546. [here]

Wager, T.D., Jonides, J., and Reading, S. (2004). Neuroimaging studies of shifting attention: a meta-analysis. Neuroimage 22, 1679–1693. [here]

Zucker (1989) Short-term synaptic plasticity. Ann. Rev. Neurosci, 12: 13-31 [here]