In this study, we used fMRI to investigate the neural correlates of spontaneous lyrical improvisation by comparing spontaneous freestyle rap to conventional rehearsed performance. Our results reveal characteristic patterns of activity associated with this novel form of lyrical improvisation and may also provide more general insights into the creative process itself. It has been suggested that the creative behaviors could occur in two stages: an improvisatory phase characterized by generation of novel material and a phase in which this material is re-evaluated and revised1. The present study may provide clues to the mechanisms that underlie the initial, improvisatory phase. Our results suggest a model in which an elementary reorganization of brain activity facilitates improvisation and may generalize to other forms of spontaneous creative behavior.

The most striking feature of lyrical improvisation detected by direct comparison of freestyle and conventional performance, in large part consistent with the previous study of melodic improvisation5, was a dissociated pattern of activity within the prefrontal cortex: increases in activity throughout the MPFC, extending from the frontal pole to the border of the pre-SMA and simultaneous decreases in the DLPFC, from its orbital to superior regions. The implications of this dissociation are discussed below, in the context of subsequent analyses.

A second salient feature of improvisation revealed by the GLM contrasts was a marked lateralization of task-related changes in the BOLD signal. For example, the medial prefrontal activations just noted were stronger in the left hemisphere, while dorsolateral prefrontal deactivations were stronger on the right. Similarly, additional task-related activations in language and motor areas were strongly lateralized to the left hemisphere, while additional deactivations in superior frontal and parietal areas were lateralized to the right.

Activation of left hemisphere language areas (in inferior frontal and posterior middle and superior temporal gyri) was predicted and is perhaps unsurprising given the nature of the genre. However it should be noted that activation here indicates enhanced activity, over and above levels observed during conventional performance and so is not related to language processing per se. Instead activation of language-related cortices likely reflects the unique demands of freestyle improvisation, which requires rapid online selection of novel words13 and phrases that rhyme14.

Increased activity in other left hemisphere regions associated with motor control (including medial and lateral premotor cortices, cingulate motor area and basal ganglia) does not appear to be related to increases in movement per se: there were no significant differences in quantitative indices of motor activity, including the number of syllables produced, during improvised and conventional conditions and no condition-dependent differences in activity of the primary motor cortex were observed. Activity in these regions may instead reflect spontaneous phonetic encoding and articulation of rapidly selected words during improvisation. Enhanced activity in the caudate may also support rapid online sequencing of ongoing behaviors in this condition15. Freestyle improvisation also requires that the articulation of words and phrases be spontaneously incorporated into established rhythmic patterns; this process might place additional demand on these regions. Additionally, both the cerebellar hemisphere and vermis, selectively activated during improvised performance, have been associated with maintenance of rhythmic patterns in working memory16. The brain regions activated in association with rhyming and rhythmic variations may provide clues to mechanisms underlying the effects of musical intervention in clinical populations17.

The widespread changes identified by the foregoing analysis are suggestive but incomplete. The questions that follow – how are these concurrent activations and deactivations related to one another; are they integrated in a meaningful way? – were addressed using connectivity analyses.

The connectivity results revealed strong positive correlations between activity in a primary seed region in the MPFC (located within in the large cluster identified in the GLM contrast, selection was guided by the results of parametric modulation analyses) and inferior frontal and cortical premotor areas. To explore the potential extensions of this network, we tracked the extended connections of the inferior frontal and premotor regions themselves. Using each as a seed in subsequent analyses, we found that these regions were themselves positively correlated with activity in the left amygdala and the amygdala itself was strongly coupled to an extended network that included the right IFG and IPL and anterior insula in both left and right hemispheres. The connectivity analyses therefore suggested the emergence of a more widespread, large-scale network that might play a role in lyrical improvisation.

Taken together, functional connectivity and GLM results provide a broader context in which to understand the dissociation of activity in medial and lateral prefrontal cortices and the ways in which this pattern might facilitate improvisation: The frontal midline cortices, selectively activated during improvisation, regulate motivational incentive, intentionality and drive18,19 and in this context the MPFC operates at the interface of intention and action – synthesizing information, encoding goals and guiding self-generated, stimulus-independent behaviors20,21,22,23,24. Normally, the expression of these behaviors is modulated by interactions between medial and lateral prefrontal regions19,25 – the MPFC provides a signal to the DLPFC, where information is processed prior to its gaining access to the motor system. In this way, the lateral prefrontal regions maintain executive control, consciously monitoring and implementing adjustments in an ongoing performance in order to ensure that actions conform to explicit goals26,27.

Here however, conventional interactions between medial and lateral prefrontal cortices appear to be markedly altered: given that BOLD signal in these regions is anticorrelated, the increases in MPFC activity appear to be tightly coupled to decreases in the DLPFC. We propose that this dissociated pattern reflects a state in which internally motivated, stimulus-independent behaviors are allowed to unfold in the absence of conscious volitional control.

There are a number of potential routes from the medial prefrontal cortex to motor effector areas in which the DLPFC could be bypassed. One parallel pathway that provides direct access to the motor system is via the dense projections from the MPFC to the CMA28,29, a premotor region that combines cognitive and affective information to orchestrate behavior.

Accordingly, we found that both the ACC and CMA (including the speech-related posterior rostral cingulate zone (RCZp)30) were significantly activated along with the MPFC during improvised performance, while activity in the DLPFC was significantly attenuated. At the same time, activity in MPFC and the cingulate areas was strongly correlated during improvised but not conventional conditions. An alternative, direct route through cingulate pathways into the motor system may allow the medial frontal regions to generate novel, exploratory behaviors31, bypassing conventional executive controls and thereby providing the cognitive flexibility necessary for successful improvisation.

It is interesting in this context that self-generated, stimulus independent behaviors appear to be initiated by midline frontal regions well before subjects consciously experience the intention to act20,32. In the absence of processing by lateral prefrontal regions – where a sense of agency could be constructed post-hoc – ongoing actions, moment to moment decisions and adjustments in performance may be experienced as having occurred outside of conscious awareness. This is not inconsistent with the experience of many artists who describe the creative process as seemingly guided by an outside agency.

In addition, the patterns we observe may reflect alterations in the activity of attentional systems: deactivations in superior portions of the DLPFC during the improvised condition (in the vicinity of the frontal eye fields) were accompanied by significant decreases in activity in the IPS. Together, these regions constitute elements of a supervisory attentional system, the so-called dorsal attention network33. This suggests that the conscious, deliberate, top-down attentional processes mediated by this network may be attenuated during improvisation, consistent with the notion that a state of defocused attention enables the generation of novel, unexpected associations that underlie spontaneous creative activity11. What monitoring and attentional processes do occur during improvisation may be mediated by the cingulate system, which remains active while DLPFC and parietal activity is reduced.

Beyond the interaction of the MPFC and DLPFC, the functional interconnections between medial prefrontal cortex, IFG, medial premotor areas and the amygdala, suggest that spontaneous lyrical improvisation is associated with emergence of a network that integrates motivation, language, emotion and motor function. The simultaneous coupling of the amygdala to inferior parietal lobules and insulae indicates that this network also incorporates regions that play a role in multimodal sensory processing and the representation of subjective experience34 and that, as a whole, this entire network is more effectively coupled during spontaneous creative behavior – perhaps facilitating what has been described as a psychological ‘flow’ state10 (which describes a subject's complete immersion in creative activity, typified by focused self-motivation, positive emotional valence and loss of self-consciousness).

Supplementary analyses revealed additional, noteworthy patterns: The results of parametric modulation analyses indicated that innovative performance – incorporation of features such as inventive wordplay or novel rhythms into the improvisation – is associated with increased activity in a subset of left hemisphere regions (Figure 2) including the posterior and middle MTG and STS and the MPFC. This suggests that regions that may correspond to the location of the mental lexicon (in which words and their semantic features are stored35, likely consistent with subjects' superior performance on verbal fluency tests) and regions that play a role in motivation, drive and self–organized behavior, may play a prominent role in the innovative use of language and rhythm. Interestingly, parametric modulation also highlighted an area not implicated in the GLM contrasts, the left posterior cingulate cortex (PCC), which has been shown to play a role, along with the MPFC, in self-motivated or self-referential behaviors36.

We also observed interesting, systematic differences in the patterns of activity in the first and last measures of the eight bar segments that constitute the basic unit of this musical form. Surprisingly we found that activity in the set of left prefrontal, premotor, anterior perisylvian language areas and amygdala reported above, was relatively higher at onset, but that activations in general appeared to shift to the right hemisphere by the final measure. This indicates first of all that the network related to motivation, emotion and language identified above may be more strongly engaged in initiating the improvisation.

What the relative increases in activity in the right hemisphere at the end of each segment indicate is however not clear. It is interesting that many of these increases were found in regions that were deactivated in the principal improvised-conventional contrast reported above. The time dependent increases in activity of frontal eye fields and IPS might reflect a re-emergence of top-down attentional processing at the end of each improvisational sequence and increasing activity in the dorsolateral prefrontal cortices might reflect an increase in executive functions mediated by these regions. It is possible that rule based behaviors (e.g. attention to metric structure, selection of final lyrical elements) may be more important and may re-engage these regulatory mechanisms, at the end of each 8 bar segment. It is clear nevertheless that the notion that simple attenuation of attention and executive control supports improvisation may be an oversimplification and that these processes seem to vary in a more complex way over time. The mechanisms underlying these interactions between musical improvisation and temporal structure clearly warrant further investigation.

As noted above, creativity may actually be a biphasic process involving initial free generation and subsequent revision of novel material1. Here we have examined only the first, spontaneous or improvisational phase. As we report, improvisation, contrasted with conventional performance, was in general associated with relative decreases in activity in supervisory attentional and executive systems. Were our subjects to actively reevaluate and revise the lyrics they had improvised, we might predict activation of these systems in support of evaluative processes that more likely require attention to and conscious, goal-directed revision of the original material. Indeed, a recent imaging study of graphic design did show activation of executive systems including the DLPFC specifically during subjects' evaluation of their prior creative outputs1.

Compared to previous studies of musical improvisation by Ullen and his colleagues4, Berkowitz & Ansari3 and Brown et al.7, our results differ in one fundamental way. While elegantly designed in order to enforce tight experimental control, these studies used conditions that were less spontaneous and may have imposed additional attentional and mnemonic demands (e.g improvised material had to be memorized as it was generated and reproduced during a subsequent scanning run4); this might in part account for the activation of the DLPFC reported in these studies. In contrast, we observed significant deactivation of the DLPFC (along with activation of the MPFC) and it is possible that this pattern may emerge when spontaneous improvisation takes place without the superimposition of secondary cognitive tasks.

In summary, the functional reorganization we observe – in which the medial prefrontal cortices may guide behavior in the absence of conscious attention and effect motor control through alternate cingulate pathways – is one feature of a larger network, linking intention, affect, language and action, that may underlie and facilitate the initial, improvisatory phase of creative behaviors. We speculate that the neural mechanisms illustrated here could be generalized to explain the cognitive processes of other spontaneous artistic forms, which can be tested in future studies across disciplines.