Displacements and linear accelerations of the head, such as those induced by tilting or translational movements (see Box A), are detected by the two otolith organs: the sacculus and the utricle. Both of these organs contain a sensory epithelium, the macula, which consists of hair cells and associated supporting cells. Overlying the hair cells and their hair bundles is a gelatinous layer, and above this is a fibrous structure, the otolithic membrane, in which are embedded crystals of calcium carbonate called otoconia (Figures 14.3 and 14.4A). The crystals give the otolith organs their name (otolith is Greek for "ear stones"). The otoconia make the otolithic membrane considerably heavier than the structures and fluids surrounding it; thus, when the head tilts, gravity causes the membrane to shift relative to the sensory epithelium (Figure 14.4B). The resulting shearing motion between the otolithic membrane and the macula displaces the hair bundles, which are embedded in the lower, gelatinous surface of the membrane. This displacement of the hair bundles generates a receptor potential in the hair cells. A shearing motion between the macula and the otolithic membrane also occurs when the head undergoes linear accelerations (see Figure 14.5); the greater relative mass of the otolithic membrane causes it to lag behind the macula temporarily, leading to transient displacement of the hair bundle. The similar effects exerted on otolithic hair cells by certain head tilts and linear accelerations explains the perceptual equivalency of these different stimuli when visual feedback is absent, as occurs in the dark or when the eyes are closed.

As already mentioned, the orientation of the hair cell bundles is organized relative to the striola, which demarcates the overlying layer of otoconia (see Figure 14.4A). The striola forms an axis of mirror symmetry such that hair cells on opposite sides of the striola have opposing morphological polarizations. Thus, a tilt along the axis of the striola will excite the hair cells on one side while inhibiting the hair cells on the other side. The saccular macula is oriented vertically and the utricular macula horizontally, with a continuous variation in the morphological polarization of the hair cells located in each macula (as shown in Figure 14.4C, where the arrows indicate the direction of movement that produces excitation). Inspection of the excitatory orientations in the maculae indicates that the utricle responds to movements of the head in the horizontal plane, such as sideways head tilts and rapid lateral displacements, whereas the sacculus responds to movements in the vertical plane (up-down and forward-backward movements in the sagittal plane). Note that the saccular and utricular maculae on one side of the head are mirror images of those on the other side. Thus, a tilt of the head to one side has opposite effects on corresponding hair cells of the two utricular maculae. This concept is important in understanding how the central connections of the vestibular periphery mediate the interaction of inputs from the two sides of the head (see next section).