Attorney David Schwarz said the question had not been raised in court previously, and he urged the panel to define authorship for copyright purposes.
The freaky legal wrangle dates from 2011 when Mr Slater was on a photographic shoot on the Indonesian island of Sulawesi.
Slater published the photos in 2014 in a book he created with software from San Francisco-based Blurb. A lower court ruled previous year that the selfie does not belong to the animal. The federal judges also chuckled at times at the novelty of the case, which involves a monkey in another country that is unaware of the fuss.
'PETA is clearly representing Naruto's best interests, ' according to the group's general counsel Jeff Kerr.
PETA says Naruto has been used to cameras throughout his life and took the selfies when he saw himself in the reflection of the lens.More news: Bryce Harper punctuates diving catch with hair flip at All-Star Game
A federal judge ruled against PETA and the monkey past year, saying he lacked the right to sue because there was no indication that Congress meant to extend copyright protection to animals.
The judges did not issue a ruling Wednesday.
The lawsuit originally included a primatologist, Antje Engelhardt, who had personally studied Naruto, as a legal next friend, but she dropped out of the case during the appeal.
The battle over a monkey selfie heads to the U.S. Court of Appeals for the Ninth Circuit in San Francisco Wednesday.
Crested macaques are part of the monkey family and have been listed as a critically endangered species by the International Union for Conservation of Nature.