OPINION ARTICLE published: 10 December 2013 BEHAVIORAL NEUROSCIENCE doi: 10.3389/fnbeh.2013.00198 Auditory and visual systems organization in 8 for gaze-shift control: where we do not see, we can hear

Marco Lanzilotto 1,2*, Vincenzo Perciavalle 3 and Cristina Lucchetti 1,2

1 Section of Physiology and Neuroscience, Department of Biomedical Sciences, Metabolic and Neuroscience, University of Modena and Reggio Emilia, Modena, Italy 2 Section of Polyclinic, Interdepartmental Facilities Center, University of Modena and Reggio Emilia, Modena, Italy 3 Section of Physiology, Department of Biomedical Sciences, University of Catania, Catania, Italy *Correspondence: [email protected] Edited by: Katharina A. Braun, Otto-von-Guericke University, Germany Reviewed by: Sophie Molholms, Albert Einstein College of Medicine, USA Keywords: FEF, PEEF, auditory system, visual system, oculomotor system, gaze shift, monkey

Hearing is especially important for most Considering all these assumptions, the visual signals into saccade motor com- primate species as they live in habitats auditory system could have an impor- mands (Schall, 1997; Sato et al., 2001). FEF of dense vegetation that limits vision. tant role to detect information even from is innervated in a topographic fashion by Stebbins (1980) summed up the evolu- regions of the space that the visual system areas of both the dorsal and ventral visual tion of the auditory system by assuming cannot explore without orienting move- streams originating in extrastriate visual that earliest mammals exploited noctur- ments. In other words, where we cannot cortex (Schall et al., 1995). The ventral nal niches since they were relatively free see, we can hear. part of the FEF receives visual information of many of the large, diurnal, predacious Through this opinion article, we argue from areas where fovea is clearly repre- reptiles. Therefore, hearing and smell were that Brodmann Area 8 receives infor- sented and retinotopically organized, such more useful at night than vision. mation from both auditory and visual as MT and V4; from areas in the infer- Our vision is limited not only in the systems and organizes a transformation otemporal cortex such as TEO and cau- dark but also outside the visual field. of these sensory signals into gaze-shift dalTEinvolvedincentralvision;finally Infact,ifweobservethebehaviorof motor commands. Our hypothesis is that from areas in parietal cortex having poor a predator like a feline, oriented toward this sensory-motor transformation is spa- retinotopic organization but important for its prey, and at the same time a sound tially organized, from both anatomical and oculomotor transformation, such as LIP. occurs behind, we might note three princi- functional points of view. In support of anatomical evidence, Suzuki pal different behaviors: the predator could Anatomical and functional properties and Azuma (1983) found that neurons maintain its gaze and ears on the prey of the Brodmann Area 8 (consisting in located in the ventral FEF had relatively neglecting the sound source; the preda- Area 8A plus Area 8B) support a medio- small visual receptive fields (RFs) repre- tor could maintain its gaze on the prey lateral organization for both auditory and senting the foveal and parafoveal regions. rotating ears and then shifting its audi- visual systems. In particular, the lateral Moreover the ventral FEF works for gen- tory attention toward the sound source; portion, corresponding to Area 8A or erating short amplitude saccades (Bruce finally the predator could break its atten- Frontal Eye Field (FEF), could play a role et al., 1985). On the contrary, the dorsal tion and orient gaze and ears toward the in receiving visual and auditory informa- part of FEF is connected with retino- sound source. A similar behavior is seen tion from a central part of the visual topically organized areas where periph- in human beings during social interaction field and then in organizing gaze-shift eral visual field is represented, such as with two or more interlocutors. motor commands toward it. Otherwise, areas MSTd and PO, located medially, In humans, orienting movements are the medial portion, corresponding to Area that are involved in peripheral vision, as carried out by the eyes, head, and/or body 8B or Premotor Ear-Eye Field (PEEF), well as from LIP. In support of anatom- operating alone or in various combina- could play a role in receiving principally ical evidence, Suzuki and Azuma (1983) tions depending on the behavioral situ- auditory information from a peripheral found that neurons located in dorsal FEF ation. However, in non-human primates, region of the space and then in organizing had larger RFs and eccentric from the such as macaque monkeys, head orienting gaze-shift motor commands toward it. fovea. Finally, the dorsal FEF is responsible movements and, more generally, gaze-shift for generating larger amplitude saccades are accompanied by ear orienting move- FRONTAL EYE FIELD (Bruce et al., 1985). ments, which allow the shifting of auditory The (FEF, area 8A) is a functional field in Otherwise, it is well known, that FEF attention toward a sound of interest (Bon the , located in the rostral receive also information from the auditory and Lucchetti, 1994, 2006; Lucchetti et al., bank of the arcuate of macaques. system, participating thus, in the trans- 2008; Lanzilotto et al., 2013; Yin, 2013). FEF participates in the transformation of formation of auditory signals into motor

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FIGURE 1 | (A) The figure represents the space detected by primates arrow represents the functional gradient discussed in the paper. Area 8A or through two different sensory modalities: green, auditory modality; red, FEF: Frontal Eye Field; Area 8B or PEEF: Premotor Ear-Eye Field; Area 9; Area visual modality. (B) Dorsal view of the monkeys’ prefrontal pole. The colored 10; IAS: Inferior Arcuate Sulcus; SAS: Superior Arcuate Sulcus. commands. An interesting study show in PREMOTOR EAR EYE FIELD a medio-lateral organization devoted for fact as FEF, in human, is a multimodal area Recently, area 8B, located medially to FEF, the exploration of different regions of involved in ultra-rapid responses for audi- has been renamed as a new frontal field: the space. In particular, the lateral part— tory and visual stimuli (Kirchner et al., PEEF (Lucchetti et al., 2008; Bon et al., which receives visual information from 2009). 2009; Lanzilotto et al., 2013). PEEF is retinotopically organized areas and has The auditory cortical system is con- characterized by having principally con- auditory neurons with RFs close to the stituted by two different streams, termed nections with the auditory system, and azimuth—could have an important role dorsal and ventral, projecting to the frontal has been hypothesized to participate in in receiving visual and auditory informa- cortex in non-human primates (Romanski the transformation of auditory signals into tion from a central region of the space et al., 1999a,b). The dorsal stream directly motor commands. In particular, PEEF is and then in organizing eye motor com- projects from caudal auditory belt to area connected directly to the caudal auditory mands toward it. On the other hand, the 8A (Romanski et al., 1999a), bringing belt through the dorsal auditory stream medial part—which receives, principally, information about sound spatial localiza- (Romanski et al., 1999a), which has a role auditory information through the dorsal tion. The ventral stream, involved in cod- for sound spatial localization. In accord to auditory stream—could have an impor- ifying the features of the auditory stimu- these connections, three principal classes tant role in receiving auditory information lus, originating from rostral auditory belt ofneuronshavebeenidentifiedinPEEF: from a peripheral region of the space and and rostral auditory parabelt, is connected auditory neurons, auditory-motor neu- then in organizing ear-eye motor com- indirectly to area 8A passing through the rons, and motor neurons. The auditory mands toward it (Figure 1). ventral prefrontal cortex (Romanski et al., stimuli that better elicit a response in 1999a; Gerbella et al., 2010; Rauschecker PEEF’s neurons are complex environmen- ACKNOWLEDGMENTS and Romanski, 2011). tal stimuli as experimenter voices, while This work was supported by Department In accord to anatomical evidence, many ear and/or eye movements represent the of Biomedical Sciences, University of neurons in FEF respond to auditory stim- motor effectors controlled by this region. Catania (“Progetti di Ricerca di Ateneo uli. FEF has an interesting medio-lateral For these reasons, PEEF has been pro- 2011”). We thank Prof. Gianfranco gradient regarding both the auditory spa- posed as a new field having a possi- Franchi for his comments. tial selectivity and proportion of auditory ble role to detect auditory stimuli in the neurons. In particular, Azuma and Suzuki space through ear and eye movements REFERENCES (1984) showed that in in the ventral part of (Lanzilotto et al., 2013). Azuma, M., and Suzuki, H. (1984). Properties and dis- FEF, auditory neurons have RFs located at tribution of auditory neurons in the dorsolateral ◦ prefrontal cortex of the alert monkey. Brain Res. 10 respect to the azimuth. As one moves CONCLUSION 298, 343–346. doi: 10.1016/0006-8993(84)91434-3 more medially toward dorsal FEF, auditory Through this opinion article, in light of Bon, L., Lanzilotto, M., and Lucchetti, C. (2009). neurons have more eccentric RFs till 40◦ PEEF discovery (Lucchetti et al., 2008; Bon “PEEF: premotor ear-eye field. A new vista of respect to the azimuth. Moreover, in dor- et al., 2009; Lanzilotto et al., 2013), we pro- area 8B,” in Prefrontal Cortex: Roles, Interventions and Traumas,edsL.LoGrassoandG.Morretti salFEFthenumberofauditoryneurons pose that the part of the frontal cortical (Portland, OR: Nova Science Publisher), 157–175. gradually increases while the number of region, consisting of area 8A (FEF) plus Bon, L., and Lucchetti, C. (1994). Ear and eye visual neurons gradually decreases. area 8B (PEEF), could be thought having representation in the frontal cortex, area 8b, of

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