This commentary is an attempt to sharpen some of the issues raised in the paper and thereby increase the generality of the proposal. Some implications of an exact definition of behavior for strategies of measurement and hence behavioral variability are discussed. The role of both respondent and operant behavior in natural selection is emphasized.

O'Regan & Noë (O&N) fail to address adequately the two most historically important reasons for seeking to explain visual experience in terms of internal representations. They are silent about the apparently inferential nature of perception, and mistaken about the significance of the phenomenology accompanying dreams, hallucinations, and mental imagery.

Rendell and Whitehead have drawn attention to some striking cetacean behaviour patterns. However, the claims for “culture” are premature. Weak examples of cetacean social learning do not, in sum, provide strong evidence for culture. Other terms, such as social learning, vocal learning, imitation, and tradition may be applied in some cases without resorting to more complex and controversial terms.

The target article proposes that visual experience arises when sensorimotor contingencies are exploited in perception. This novel analysis of visual experience fares no better than the other proposals that the article rightly dismisses, and for the same reasons. Extracting invariants may be needed for recognition, but it is neither necessary nor sufficient for having a visual experience. While the idea that vision involves the active extraction of sensorimotor invariants has merit, it does not replace the need for perceptual representations. Vision is not just for the immediate controlling of action; it is also for finding out about the world, from which inferences may be drawn and beliefs changed.

The target article provides stimulating evidence for culture in cetaceans but does not provide a coherent theoretical framework. We argue that a complex, adaptive systems approach not only can provide such a framework but also can contribute advanced data analysis and simulation methods. For humpback whale songs, we suggest the framework of “small-world networks” to model the observed spatio-temporal dynamics.

Hull et al.'s construction of operant learning as an instance of selection gives rise to problems that weaken this application of selection theory beyond acceptable limits. We point out that most fundamental is a disregard for the need to include multiple concurrent replicators in any definition of selection and indicate how this problem may be solved.

We agree with Rendell and Whitehead that cetaceans acquire knowledge from caretakers and peers, and that a clear understanding of this process can provide insight into the evolution of mammalian cognition. The passive observational methods they advocate, however, are inadequate for determining what cetaceans know. Only by experimentally investigating the cognition of cetaceans can we hope to understand what they learn through social interactions.

Activity anorexia illustrates selection of behavior at the biological, behavioral, and neural levels. Based on evolutionary history, food depletion increases the reinforcement value of physical activity that, in turn, decreases the reinforcement effectiveness of eating – resulting in activity anorexia. Neural opiates participate in the selection of physical activity during periods of food depletion.

O'Regan & Noë (O&N) are pessimistic about the prospects for discovering the neural correlates of consciousness. They argue that there can be no one-to-one correspondence between awareness and patterns of neural activity in the brain, so a project attempting to identify the neural correlates of consciousness is doomed to failure. We believe that this degree of pessimism may be overstated; recent empirical data show some convergence in describing consistent patterns of neural activity associated with visual consciousness.

The research program defended by O'Regan & Noë (O&N) cannot give any plausible explanation for the fact that during REM-sleep the brain regularly generates subjective experiences (dreams) where visual phenomenology is especially prominent. This internal experience is almost invariably organized in the form of “being-in-the-world.” Dreaming presents a serious unaccountable anomaly for the sensorimotor research program and reveals that some of its fundamental assumptions about the nature of consciousness are questionable.

An analysis of biological selection aimed at deriving a mechanism-independent definition removes Hull et al.'s obligatory requirement for replication of the carriers of information, under conditions, such as those obtaining in the nervous system, where the information content of a carrier can be modified without duplication by an amount controlled by the outcome of interactions with the environment.

Results of genetic analyses show that social groups of female and immature sperm whales are comprised of multiple matrilines as evidenced by the presence of multiple mitochondrial (maternally inherited) control region haplotypes. These data suggest: (1) a social environment in which the transmission of cultural information, such as vocal dialects, is more likely to be horizontal or oblique rather than strictly vertical (mother-offspring) and (2) lead us to question the data presented to support gene-culture coevolution.

The interaction of the organism with the environment requires not only reactive, but also active behavior (i.e., search activity) which helps subject to meet the challenge of the uncertainty of the environment. A positive feedback between active behavior and immune system makes the selection process effective.

Rendall and Whitehead overstate the weak evidence for social learning in cetaceans as a group, including the current evidence for vocal learning in killer whales. Ethnographic techniques exist to test genetic explanations of killer whale calling behavior, and additional captive experiments are feasible. Without such tests, descriptions of learning could be considered pseudo-scientific, ad hoc auxiliary assumptions of an untested theory.

Two cross-modal experiments provide partial support for O'Regan & Noë's (O&N's) claim that sensorimotor contingencies mediate perception. Differences in locating a target sound accompanied by a spatially disparate neutral light correlate with whether the two stimuli were perceived as spatially unified. This correlation suggests that internal representations are necessary for conscious perception, which may also mediate sensorimotor contingencies.

The types of cetacean cultural behavior patterns described (primarily food-related and communication-related) reflect a very different research focus than that found in primatology, where dietary variation and food processing is emphasized and other potentially “cultural” patterns have (until recently) been relatively neglected. The lack of behavioral research in all but a few cetacean species is also notable, as it mirrors a bias in primatology towards only a few genera.

Although O'Regan & Noë (O&N) claim that the world may serve as the viewers' external visual memory, findings from the field of memory research have demonstrated the existence of internal visual representations. These representations are stored in the viewer's brain, contain information regarding visual objects and their relations, guide subsequent exploration of the visual world and promote change detection.

Campbell (1960) proposed a “blind-variation and selective retention” model of creative cognition. Subsequent researchers have developed this BVSR model into a comprehensive theory of human creativity, one that recognizes that human creativity operates by more than one cognitive process. The question is then raised of how the BVSR model can be accommodated within the Hull et al. selectionist system.

Hull et al. make a direct connection between selection and replication. My view is that selection, at its causal crux, is not inherently connected to replication. I make plain the causal crux of selection, distinguishing it from replication. I discuss implications of my results for Hull et al.'s critique of Darden and Cain (1989).

Defining culture as social learning means that culture is present in many birds and mammals, suggesting that cetacean culture is not so special and does not require special explanation. Contrary to their own claims, Rendell and Whitehead present culture as having variant forms in different species, and these forms seem inconsistently applied and compared across species.