We agree with Block's hypothesis that phenomenally conscious states may sometimes not be cognitively accessible. Partial report and dual-tasks paradigms show that we have only limited access to some aspects of phenomenal experience. Or, to adopt Block's earlier language, phenomenal consciousness can occur without access consciousness, a revision of our earlier position (Crick & Koch Reference Crick1998a; Koch Reference Koch2004). We argue here that sensory psychology has a long-standing framework to consider such cases, involving attentional selection processes.

We recently (Koch & Tsuchiya Reference Koch and Tsuchiya2007; Tsuchiya & Koch Reference Tsuchiya, Koch, Laureys and Tononi2008) summarized the empirical evidence that consciousness and top-down, volitionally controlled endogenous attention are distinct neurobiological processes with distinct functions (see also, Iwasaki Reference Iwasaki1993; Lamme Reference Lamme2003). In particular, sensitive psychophysical techniques can dissociate these two. Indeed, a range of phenomena exists in which subjects are conscious of certain stimuli attributes without top-down attention. This list includes the pop-out target in a visual search task, gist perception of a scene, categorization of peripheral targets when a very intensive cognitive-resource task has to be performed at fixation, and iconic memory.

Consider Sperling's original iconic memory experiment (Sperling Reference Sperling1960) or Landman et al.'s (Reference Landman, Spekreijse and Lamme2003) variant. Subjects report that they clearly, vividly, and consciously see a field of letters or a bunch of bars arranged on a circle. This is also what we experience when we look at such displays. However, it is well known that subjects have only very limited access to the detailed properties of the individual elements, unless top-down attention is directed to a subset of stimuli using appropriately timed cues. Our basic point is that phenomenology without conscious access is an example of consciousness without top-down attention processing, though the converse is not true; that is, not every example of conscious perception in the absence of top-down attention is cognitively non-accessible. For example, the gender of a briefly presented face can be accurately reported even if subjects are engaged in a highly demanding task at the fixation (Reddy et al. Reference Reddy, Wilken and Koch2004).

So what is the story at the level of the brain? Decades of electrophysiological recordings in monkeys have proven that the spiking response of neurons in the ventral visual stream (e.g., in areas V4 and IT) representing attended stimuli is boosted at the expense of the response to non-attended items. According to Crick and Koch (Reference Crick and Koch1995), this enables these neurons to establish a reciprocal relationship with neurons in the dorsolateral prefrontal cortex and related regions that are involved in working memory and planning (and language in humans), leading to reverberatory neuronal activity that outlasts the initial stimulus duration. Critical to the formation of such a single and integrated coalition of neurons are the long-range axons of pyramidal neurons that project from the back to the front of cortex and their targets in the front that project back to the upper stages of the ventral pathway (possibly involving stages of the thalamus, such as the pulvinar [Crick & Koch Reference Crick1998b], and the claustrum [Crick & Koch Reference Crick2005]). The subject now consciously sees these stimuli and can report on their character (e.g., identify the letter [Sperling 1960] or the orientation of the square [Landman et al. Reference Landman, Spekreijse and Lamme2003]). Furthermore, the subject also has a strong conscious sense of the entire scene (“I see an array of letters”) that is likewise mediated by a loop that involves the inferior temporal cortex and the frontal lobes half-way across the brain.

But what happens to those stimuli that do not benefit from attentional boosting? Depending on the exact circumstances (visual clutter in the scene, contrast, stimulus duration) these stimuli may likewise establish coalitions of neurons, aided by local (i.e., within the cortical area) and semi-local feedback (i.e., feedback projections that remain consigned to visual cortex) loops. However, as these coalitions of neurons lack coordinated support from feedback axons from neurons situated in the prefrontal cortex, thalamus, and claustrum, their firing activity is less vigorous and may decay much more quickly. Yet, aided by the neuronal representation of the entire scene, these weaker and more local coalitions may still be sufficient for some phenomenal percepts.

Block cites functional magnetic resonance imaging (fMRI) studies of patients with visuospatial hemi-neglect (Driver & Vuilleumier Reference Driver and Vuilleumier2001; Rees et al. Reference Rees, Wojciulik, Clarke, Husain, Frith and Driver2000; Reference Rees, Wojciulik, Clarke, Husain, Frith and Driver2002b) that offer evidence of enhanced hemodynamic activity in the fusiform face area contralateral to a face that the patient is not aware of. For Block, this raises the question of whether this is likewise an example of phenomenal consciousness without cognitive access. We answer this question clearly in the negative. First, one should trust the first-person perspective: That is, in the absence of compelling, empirical evidence to the contrary (such as Anton's blindness, also known as hysterical blindness; Sackeim et al. Reference Sackeim, Nordlie and Gur1979), if the subject denies any phenomenal experience, this should be accepted as a brute fact. If we take the existence of mere recurrent, strong neuronal activation as evidence for consciousness, why not argue that the spinal cord or the enteric nervous system is conscious but is not telling me (Fearing Reference Fearing1970)? Second, the relationship between neuronal firing activity and the associated hemodynamic BOLD response is a very complex one. In particular, there are well-documented cases where a vigorous fMRI signal is observed in the absence of any spiking from the principal neurons in that area (Harrison et al. Reference Harrison, Harel, Panesar and Mount2002; Logothetis Reference Logothetis2003; Logothetis & Wandell Reference Logothetis and Wandell2004; Mathiesen et al. Reference Mathiesen, Caesar, Akgoren and Lauritzen1998). Synaptic activity is a much larger driver of hemodynamic activity than are action potentials. Therefore, a much more cautious reading of these studies is that they demonstrate synaptic input into the fusiform face area in these patients; however, whether or not this input is vigorous enough to establish a sustained coalition of neurons is totally up in the air and requires further investigations.

In conclusion, the quiddity of the neuronal correlates of conscious access are long-range loops between the back and the front of cortex and its associated satellites (thalamus, basal ganglia and claustrum), enabled by top-down attention. Without this amplification step, most coalitions in the back are fated to die; however, given the right conditions, a few may survive and may be consciously experienced by the subject. Yet, as the informational content of these coalitions are not accessible to working memory and planning circuits in the front, the subject cannot consciously access the detailed stimulus attributes. Our explanation provides a plausible account of how phenomenal consciousness can occur without cognitive access.