Here we show that two blind individuals can use echolocation to determine the shape, motion and location of objects with great accuracy, even when only listening passively to echolocation sounds that were recorded earlier. When these recordings were presented during fMRI scanning, we found that ‘visual’ cortex was strongly activated in one early blind participant (EB) and to a lesser degree in one late blind participant (LB). Most remarkably, the comparison of brain activity during sounds that contained echoes with brain activity during control sounds that did not contain echoes revealed echo related activity in calcarine, but not auditory cortex.
The question arises if the activity that we observe in calcarine cortex is truly related to echolocation, or if it is simply due to the fact that EB and LB are blind. Blindness can result in re-organization of many brain areas, including but not limited to visual, auditory and somatosensory cortex and subcortical structures, even though the underlying mechanism and exact nature of the changes are still unclear 
. Based on the existing literature, therefore, it is not surprising to see activity in visual cortex in response to auditory stimuli in EB and LB. However, support for an interpretation of the activation in terms of echolocation, but not blindness per se, is provided by the outdoor scenes experiment, in which we see differential activation in calcarine cortex in EB and LB, but not in auditory cortex when echoes are present (or not) in the outdoor sounds (). In this regard our data go beyond ‘classical’ cross-modal results that show co-activation of visual cortex and areas primarily sensitive to the stimulus (i.e. primary auditory or somatosensory cortex). In a related point, we want to emphasize that the differences in the level of activation in the visual areas of EB's and LB's brains could have arisen for a number of reasons. First, there might be differences in cortical development in the two individuals; after all, EB lost his sight much earlier than LB. Second, EB started using echolocation as a small child and has used it longer than LB. A consequence of this might be that EB creates a more vivid representation of the spatial scene from click-echoes. Third, EB performed better in the passive-listening paradigm than LB even though this difference was reduced for ‘outdoor’ sound recordings. But of course, any combination of all these factors could account for the differences in the activity in visual areas we observed in these two individuals.
It would be useful in future neuroimaging studies of echolocation to include sighted people who have been trained to echolocate, or blind people who have a ‘regular’ sensitivity to echoes. With respect to the latter, there is evidence that blind people, even when they do not consciously echolocate, are more sensitive to echoes than sighted people 
, and this might pose a challenge when comparing the brain activation of self-proclaimed echolocators to the brain activation of self-proclaimed non-echolocators who are also blind. In any case, the comparison we draw here (i.e. between blind echolocators and sighted non-echolocators) is insightful, because it highlights the involvement of visual rather than auditory cortex in the processing of echoes.
The patterns of activation observed in their brains might shed some light on the possible role that sensory deprivation plays in the recruitment of visual cortex during echolocation in the blind. On the behavioural level, of course, sighted people's echolocation abilities have been repeatedly shown to be inferior to those of blind people (for reviews see 
). There are various reasons why this is the case. One possibility is that blind people use echolocation on a daily basis and therefore acquire a higher skill level through practice. Another possibility might be that blind people have better hearing abilities which may also make them better at echolocation, e.g. 
. Our current data suggest that hearing ability is not a variable, because both EB and LB performed within the normal range on standard hearing and source localization tests (Figure S1
; Audiology Report S1
). Furthermore, we also saw no obvious differences in activation in auditory cortex between EB and LB or between these two individuals and the control participants (, Figure S3
). It cannot be ruled out, however, that the tests and comparisons we used are not suitable for detecting the auditory abilities that may underlie superior echolocation performance. Finally, it is also possible that sighted individuals might simply be at a disadvantage in acquiring echolocation skills, because echolocation and vision compete for neural resources. Clearly, more investigations of human echolocation are needed on the behavioural, computational, and neural level, to uncover how echolocation works, how it is acquired and which neural processes are involved.
It is important to emphasize that the use of echolocation in the blind goes well beyond localizing objects in the environment. The experts we studied were also able to use echolocation to perceive object shape and motion – and even object identity. In addition, they were able to use passive listening with 10-kHz cut-off to do these kinds of tasks – which made it possible for us to probe neural substrates of their abilities. Clearly more work is needed comparing performance with active and passive echolocation across a range of different tasks – where the available frequency ranges in both conditions are systematically varied.
It could be argued that the contralateral bias that we observed in EB's calcarine cortex reflects differences in spatial attention between the two conditions. Effects of attention on brain activity have been shown for visual 
, as well as other cortical areas, including auditory cortices, e.g. 
. Thus, although we cannot rule out this explanation, it would still be remarkable that EB, who lost his eyes when he was 13 months of age, would show attentional modulation of the calcarine cortex, but not the auditory cortex – and would do this in a contralateral fashion.
Both EB and LB show BOLD activity in temporal cortical regions typically devoted to motion processing, but this activity is absent in C1 and C2. In a similar fashion, both EB and LB reported to perceive motion, but this percept was absent in C1 and C2. Thus, we see good correspondence in terms of brain activity and perception. The question remains, however, as to what the ‘preferred modality’ of the neurons is that are active in EB and LB when they perceive motion using echolocation. Neurons adjacent and inferior to the ITS/LOS junction are sensitive to both visual and auditory motion as determined with functional localization techniques 
. Sighted individuals typically show a modality specific cortical organization, such that neurons that are sensitive to visual motion (i.e. area MT+) are located adjacent but posterior to neurons that are sensitive to auditory motion 
. In contrast, individuals who regained vision at a later point in their life (i.e. late onset sight recovery) show cortical organization that is not modality specific, such that visual and auditory motion areas largely overlap 
. Finally, neurons in and around visual motion area MT+ may also respond to tactile motion, even though it remains to be determined to what degree this activity is potentially mediated by visual imagery 
. Future research is needed to investigate how neurons that are active during echolocation motion correspond to visual motion area MT+ in sighted people.
An obvious question that arises from our findings is what function calcarine cortex might serve during echolocation. One possibility is that it is involved in the comparison between outgoing source sound (e.g. mouth click) and incoming echo. This explanation seems unlikely, however, because if the calcarine computed a comparison between outgoing source sound and incoming echo, it would also compute that comparison in the absence of echoes. If that were the case, however, we would expect the calcarine to be equally active in the presence and the absence of echoes – provided the corresponding clicks were present. The pattern of activity we found in EB and LB does not support this interpretation (). An alternative, and perhaps more plausible, explanation is that calcarine cortex performs some sort of spatial computation that uses input from the processing of echolocation sounds that was carried out elsewhere, most likely in brain areas devoted to auditory processing. In this case, one would expect calcarine cortex to be more active in the presence than in the absence of echoes, because the trains of sounds with echoes contain more spatial information than those without echoes. The activity patterns we found in EB and LB would certainly support this interpretation (). We are not the first to propose that visual cortex could potentially subserve ‘supra-modal’ spatial functions after loss of visual sensory input 
. Recently, a similar supra-modal spatial function has also been suggested for certain parts of auditory cortex after loss of auditory sensory input 
. Again, future research is needed to determine exactly how activity in calcarine cortex mediates echolocation.
The cerebellar structures linked to visual sensory processing 
also appear to play a role in echolocation in the blind. In particular, we found that lobule X is more active in both EB and LB during echolocation than during control sounds. Thus, the arguments discussed above for potential function of calcarine cortex during echolocation also apply to lobule X.
In addition to lobule X, we also found activity in left lobule VIIAt/Crus II during echolocation. Since this part of the cerebellum is involved in a non-motor loop involving Brodmann area 46 in pre-frontal cortex 
, the co-activation that we see in this part of the cerebellum and in cortex adjacent and inferior to the right middle frontal sulcus makes sense. As a caveat, we want to note however, that we cannot be certain that the activity we found adjacent and inferior to the middle frontal sulcus actually corresponds to activity in Brodmann area 46, because there is natural variability in the anatomical location of Brodmann area 46 in the human brain 
. In any event, we suggest that the activation of right middle prefrontal cortex and left cerebellar lobule VIIAt/Crus II most likely reflects the involvement of cognitive and executive control processes that are non-echolocation specific. This hypothesis is supported by the fact that we also saw activity in these brain areas in C1 and C2. It is unlikely that this activity reflects motor imagery or the activation of a ‘click motor-scheme’ during the passive listening paradigm, because the click sound was the same between outdoor echo and outdoor control stimuli where only the echo was missing.
The current study is the first to investigate which brain areas potentially underlie natural echolocation in early- and late-blind people (EB and LB). In EB, we found robust echolocation-specific activity in calcarine cortex – but not in auditory cortex. A similar pattern was observed in LB, but the activity in the calcarine cortex was not as extensive. We also found that the calcarine activity was greater for echoes reflected from surfaces located in contralateral space in EB but not LB. Our findings also shed new light on how the cerebellum might be involved in sensory processing. In addition, our study introduced novel methodology that can be used in future experiments on echolocation.
From a more applied point of view, our data clearly show that EB and LB use echolocation in a way that seems uncannily similar to vision. In this way, our study shows that echolocation can provide blind people with a high degree of independence and self-reliance in their daily life. This has broad practical implications in that echolocation is a trainable skill that can potentially offer powerful and liberating opportunities for blind and vision-impaired people.