Neuronal mechanisms of novelty seeking

Abstract

Humans and other primates interact with the world by observing and exploring visual objects. In particular, they often seek out the opportunities to view novel objects that they have never seen before, even when they have no extrinsic primary reward value. However, despite the importance of novel visual objects in our daily life, we currently lack an understanding of how primate brain circuits control the motivation to seek out novelty. We found that novelty-seeking is regulated by a small understudied subcortical region, the zona incerta (ZI). In a task in which monkeys made eye movements to familiar objects to obtain the opportunity to view novel objects, many ZI neurons were preferentially activated by predictions of future novel objects and displayed burst excitations before gaze shifts to gain access to novel objects. Low intensity electrical stimulation of ZI facilitated gaze shifts, while inactivations of ZI reduced novelty-seeking. Surprisingly, additional experiments showed that this ZI-dependent novelty seeking behavior is not regulated by canonical neural circuitry for reward seeking. The habenula-dopamine pathway, known to reflect reward predictions that control reward seeking, was relatively inactive during novelty-seeking behavior in which novelty had no extrinsic reward value. Instead, high channel-count electrophysiological experiments and anatomical tracing identified a prominent source of control signals for novelty seeking in the anterior ventral medial temporal cortex (AVMTC), a brain region known to be crucially involved in visual processing and object memory. In addition to their well-known function in signaling the novelty or familiarity of objects in the current environment, AVMTC neurons reflected the predictions of future novel objects, akin to the way neurons in reward-circuitry predict future rewards in order to control reward-seeking. Our data uncover a network of primate brain areas that regulate novelty-seeking. The behavioral and neural distinctions between novelty-seeking and reward-processing highlight how the brain can accomplish behavioral flexibility, providing a mechanism to explore novel objects.

Striatal dopamine explains novelty-induced behavioral dynamics and individual variability in threat prediction

“…Thus, the degree of shaping bonus may determine whether an agent becomes neophobic or not. This is different from forced familiarization in many studies (Menegas et al, 2018; Morrens et al, 2020; Ogasawara et al, 2021) and in the pre-exposure in our experiments. In forced familiarization, animals cannot totally avoid an object and so continue to learn and update threat prediction.…”

“…Importantly, the canonical dopamine system – those that project from the ventral tegmental area (VTA) to the ventral striatum (VS) – does not respond to novel stimuli at the population level (Menegas et al, 2017). Recent studies in monkeys also found that dopamine neurons in substantia nigra pars compacta (SNc) do not respond to novelty per se (Ogasawara et al, 2021), but rather respond to novelty in the context of information seeking for reward (Bromberg-Martin and Hikosaka, 2009). In contrast, recent studies found that dopamine neurons that project to the tail of the striatum (TS) or the prefrontal cortex play a role in task-independent novelty-related behaviors (Menegas et al, 2018; Morrens et al, 2020).…”

“…However, individual variability is an important factor to understand the neural computations (Marder and Goaillard, 2006). Secondly, many previous studies were conducted in constrained environments that limited behavioral choices (Menegas et al, 2017; Morrens et al, 2020; Ogasawara et al, 2021). It has been reported that animals respond differently to novel objects depending on whether the animal is in a small environment (“forced exposure”) or in a sufficiently large enclosure to be able to choose between exploring or totally avoiding a novel object (“voluntary exploration”) (Corey, 1978; Rebec et al, 1997).…”